(Coral Reefs of the World 9) Covadonga Orejas, Carlos Jiménez - Mediterranean Cold-Water Corals_ Past, Present and Future_ Understanding the Deep-Sea Realms of Coral-Springer International Publishing

Coral Reefs of the World 9
Covadonga Orejas
Carlos Jiménez Editors
Mediterranean
Cold-Water Corals:
Past, Present
and Future
Understanding the Deep-Sea Realms of Coral
Coral Reefs of the World
Volume 9
Series editors:
Bernhard M. Riegl, Nova Southeastern University, Dania Beach, USA
Richard E. Dodge, Nova Southeastern University, Dania Beach, USA
Coral Reefs of the World is a series presenting the status of knowledge of the world’s coral
reefs authored by leading scientists. The volumes are organized according to political or
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Covadonga Orejas • Carlos Jiménez
Editors
Mediterranean Cold-Water
Corals: Past, Present and
Future
Understanding the Deep-Sea Realms
of Coral
Editors
Covadonga Orejas Carlos Jiménez
Instituto Español de Oceanografía (IEO) Enalia Physis Environmental Research Centre
Centro Oceanográfico de Baleares (ENALIA)
Palma de Mallorca, Spain Nicosia, Cyprus
ISSN 2213-719X ISSN 2213-7203 (electronic)

Coral Reefs of the World
ISBN 978-3-319-91607-1 ISBN 978-3-319-91608-8 (eBook)
https://doi.org/10.1007/978-3-319-91608-8
Library of Congress Control Number: 2018954937
© Springer International Publishing AG, part of Springer Nature 2019

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to Wolf Isbert for his continuous support in the gestation and completion of
this volume.
to Helmut Zibrowius for mentoring and teaching the sorcerer’s apprentice
into the Mediterranean marine ecology.
Foreword
Spend any time working on cold-water corals and you will quickly find yourself, like the corals
themselves, at the confluence of ocean physics, geology, chemistry and biology. This meeting
of disciplines is beautifully explored in the diverse chapters of this book where Covadonga
Orejas and Carlos Jiménez have carefully selected an impressive collection of contributions
spanning the past, present and future of Mediterranean cold-water corals.
The very word Mediterranean derives from the Latin “in the middle of land”, and this
almost land-locked sea has long fascinated marine scientists. The relatively small volume and
rapid overturning circulation patterns of its waters make the Mediterranean an intriguing loca-
tion to follow the implications of global climatic change from ocean warming to acidification.
Its present biodiversity and biogeography reflects the imprint of major climatic changes from
the severity of the Messinian Salinity Crisis, when the entire basin was cut from the Atlantic,
through to its recolonisation over subsequent millennia. Much later during the last glaciation,
while northern latitudes were under ice and the Atlantic’s overturning circulation slowed, it is
highly likely that the Mediterranean provided refuge for some of the cold-water corals today
most abundant in the Atlantic Ocean. Our understanding of this fascinating history is far from
complete, but the revolution in our abilities to accurately date fossil coral remains and trace
genetic lineages with next-generation sequencing approaches mean the pieces of this compli-
cated jigsaw are gradually being assembled.
The Mediterranean also has a very special place in the history of cold-water coral research.
In popular culture the word coral is often linked to the coral jewellery produced since antiquity
from skeletons of the Mediterranean precious coral Corallium rubrum, a practice that has
sadly had severe consequences for today’s Corallium populations. Linnaeus described the
scleractinian Madrepora oculata from samples taken from the central Mediterranean and
Tyrrhenian Sea and some of the best-preserved fossil reef occurrences of the iconic Atlantic
framework-former Lophelia pertusa are found on islands like Rhodes and Crete. Indeed, it was
until relatively recently that it seemed the Mediterranean no longer supported substantial live
cold-water coral reef habitats. At the turn of the twenty-first century I vividly remember the
excitement when the Santa Maria di Leuca coral mounds were first discovered in the northern
Ionian Sea – reversing the accepted wisdom that the Mediterranean had become a graveyard
for living reefs of Lophelia, Madrepora and Desmophyllum.
Thus, the Mediterranean holds a special place for deep coral researchers, particularly those
working in the Atlantic. We cannot understand the interconnectivity of today’s Atlantic cold-
water coral habitats if we do not understand their wider relationships to neighbouring sea
basins, especially those that formed important glacial refugia. This book is being published
half way through one of the most ambitious attempts to understand deep-water ecosystems,
including cold-water corals, at the scale of the North Atlantic Ocean. The European Horizon
2020 ATLAS project (2016–2020) brings together over 120 researchers from Europe, Canada
and the USA with the shared objective of producing a transatlantic assessment of deep-water
ecosystems and developing integrated ecosystem-based spatial management plans for their
long-term conservation and management. It is telling that the second dedicated ATLAS
research cruise in 2016 was the MEDWAVES expedition that sailed from the Strait of Gibraltar
to the Azores and back again to follow the influence of Mediterranean outflow water on the
vii
viii Foreword
biodiversity and biogeography of cold-water corals and other key taxa on Atlantic seamounts
and offshore banks.
As I write this it is simply fantastic to reflect upon how much has been achieved since the
renaissance of cold-water coral research in the Mediterranean began, arguably kick-started
with the discovery of the Santa Maria di Leuca coral mounds 18 years ago. We now know so
much more about the diversity of Mediterranean cold-water coral habitats from these deep reef
frameworks through to the habitats associated with dramatic canyons, mysterious mud volca-
noes and beautiful coral gardens of delicate antipatharian and gorgonian corals. We know more
about how important they are in the ecology of other species, notably fish, and are starting to
really understand how these corals are intimately linked with surface productivity and tight
coupling of that primary productivity to supply food via dynamic near-bed currents. We are
beginning to reveal just how important the archives locked in the chemistry of coral skeletons
will be in helping us to understand past environmental conditions, a resource we badly need to
understand as we move further into the Anthropocene and truly unparalleled rates of environ-
mental change.
Huge congratulations are due to everyone involved in this book, a book important not just
for the Mediterranean but for cold-water coral researchers across the world.
Head Changing Oceans Research Group J. Murray Roberts

School of GeoSciences
University of Edinburgh
Edinburgh, UK
January, 2019
Acknowledgements
This book is an eclectic selection of topics that encompass the knowledge of the past, present
and future of the Mediterranean cold-water corals. It draws on the help and time of many
people. We are in debt to our families and friends for the many hours stolen from the “theoreti-
cal” free-time and weekends with them and for delaying and delaying once again visits and
holidays. Thanks to you all for your understanding and continuous support, for your patience
and for being there!
We also would like to express our gratitude to Springer for granting their trust in us for this
adventure, in particular we would like to express our thanks to Alexandrine Cheronet and
Judith Terpos who gave us excellent support and advice during the entire process. Thanks for
your enthusiasm and also for being patient and accepting our proposal of the “drop” chapters,
and for allowing us as well to introduce a new concept for the book’s cover thanks to Autun
Purser, who provided us with a stunning drawing. Our colleague Christine Ferrier-Pagès
(Scientific Centre of Monaco) had a paramount role in this book concept and its inception,
thanks Christine for your trust and support! Also special thanks to Marco Taviani (Instituto di
Scienze Marine, Bologna). Marco was one of the main inspirational characters for this book,
not only by participating in several chapters but also providing ideas and suggestions all very
useful for Carlos and me.
A book of these characteristics cannot be constructed without the help of altruist, engaged,
dedicated and very, very patient reviewers, from those we got more than 80 in this project, our
biggest thanks go to: Agostina Vertino, Alessandro Cau, André Freiwald, Andrea Gori, Andrea
Peirano, Andrés Rüggeberg, Aneleen Foubert, Antonieta Rosso, Branko Velimirov, Bruno
Sabelli, Marina Carreiro-Silva, Cheryl Morrison, Claudia Pichler, Claudia Wienberg, Claudio
Lo Iacono, Cristina Linares, David Johnson, Dierk Hebbeln, Di Tracey, Eleonora Martorelli,
Eric Douville, Ester Serrao, Federica Constantini, Gemma Ercilla, Jarek Stolarski, Jordi
Grinyó, José Templado, Juancho Movilla, Jürgen Titschack, Kathleen Roberts, Christina
Kellog, Lehne Buhl-Mortensen, Luís Pinheiro, Marco Roveri, Marco Taviani, Marie Claire
Fabri, Marín, Marina Carreiro-Silva, Mark Wilson, Marzia Bo, Nadia Santodomingo, Nadine
Le Bris, Paolo Montagna, Patric Schembri, Rana Abu Alhaija, Ricardo Aguilar, Ronald Osinga,
Sandra Brooke, Sebastian Hennige, Sergio Rossi, Simone Pietro Canese, Sophie Arnaud-
Haond, Stephan Ekehaug, Stephanie Reynaud, Thierry Baussant and many more who decided
to remain anonymous.
We feel really honoured having the collaboration of Prof. Murray Roberts in this book.
Murray Roberts is one of the big names in the cold-water coral research world, a reference
scientist in the field, and a very good friend. Many thanks, Murray, for your continuous support
and interest in this volume and for being willing to write the foreword.
Frequently, the “helping hands in the shadow” are paramount to conclude a project (for us
a big project) like this one. Among these hands, the two from Wolf Isbert were fundamental,
especially in the last weeks before finishing the volume. Wolf many thanks for your vital help,
support … thanks for being always there!
Finally, we are grateful that we can work in the topic which is also our passion: the sea and
its creatures. Carlos and I are enthusiastic coral devotees, and it is a privilege to have the
opportunity to explore, discover and investigate these fascinating creatures and habitats. The
ix
x Acknowledgements
privilege is double if the passion can be shared with friends as we have been able to do for this
book.
This work is a contribution to the ATLAS project and has received funding from the
European Union’s Horizon 2020 research and innovation programme under Grant Agreement
No. 678760. It reflects the author’s views, and the European Union is not responsible for any
use that may be made of the information it contains
Contents
Introduction
1 An Introduction to the Research on Mediterranean Cold-Water Corals............ 3
Covadonga Orejas and Carlos Jiménez
Part I Past
2 Paleoecology of Mediterranean Cold-Water Corals.............................................. 15
Marco Taviani, Agostina Vertino, Lorenzo Angeletti, Paolo Montagna,
and Alessandro Remia
3 Cold-Water Corals in the Mediterranean: A History of Discovery...................... 31
Julian Evans, Leyla Knittweis, Joseph A. Borg, and Patrick J. Schembri
4 A Turbulent Story: Mediterranean Contourites and Cold-Water Corals........... 35
Michele Rebesco and Marco Taviani
5 Messinian Salinity Crisis: What Happened to Cold-Water Corals?.................... 47
André Freiwald
6 Did Quaternary Climate Fluctuations Affect Mediterranean
Deep-Sea Coral Communities?................................................................................ 51
Agostina Vertino and Cesare Corselli
7 A Deglacial Cold-Water Coral Boom in the Alborán Sea:
From Coral Mounds and Species Dominance........................................................ 57
Claudia Wienberg
8 Highly Variable Submarine Landscapes in the Alborán Sea
Created by Cold-Water Corals................................................................................ 61
Dierk Hebbeln
9 Spatio-Temporal Distribution of Mediterranean Cold-Water Corals................. 67
Agostina Vertino, Marco Taviani, and Cesare Corselli
10 Bathyal Corals Within the Aegean Sea and the Adjacent Hellenic Trench......... 85
Jürgen Titschack
11 Mediterranean Cold-Water Corals as Paleoclimate Archives.............................. 95
Paolo Montagna and Marco Taviani
12 Tomography of Cold-Water Corals-Bearing Cores............................................... 109
Lorenzo Angeletti, Matteo Bettuzzi, and Maria Pia Morigi
13 Changing Views About Mediterranean Cold-Water Corals................................. 115
Marco Taviani
xi
xii Contents
Part II Present
14 Taxonomy, Genetics and Biodiversity of Mediterranean
Deep-Sea Corals and Cold-Water Corals............................................................... 121
Alvaro Altuna and Angelo Poliseno
15 Habitat Mapping of Cold-Water Corals in the Mediterranean Sea..................... 157
Claudio Lo Iacono, Alessandra Savini, Veerle A. I. Huvenne,
and Eulàlia Gràcia
16 Cold-Water Coral Habitat Mapping in the Mediterranean Sea:
Methodologies and Perspectives.............................................................................. 173
Lorenzo Angeletti, Annaëlle Bargain, Elisabetta Campiani,
Federica Foglini, Valentina Grande, Elisa Leidi, Alessandra Mercorella,
Mariacristina Prampolini, and Marco Taviani
17 Working with Visual Methods, Comparison Among
the French Deep-Sea Canyons................................................................................. 191
Maïa Fourt, Adrien Goujard, and Pierre Chevaldonné
18 Review of the Circulation and Characteristics of Intermediate
Water Masses of the Mediterranean: Implications for Cold-Water
Coral Habitats........................................................................................................... 195
Daniel R. Hayes, Katrin Schroeder, Pierre-Marie Poulain, Pierre Testor,
Laurent Mortier, Anthony Bosse, and Xavier du Madron
19 Occurrence and Biogeography of Mediterranean Cold-Water Corals................ 213
Giovanni Chimienti, Marzia Bo, Marco Taviani, and Francesco Mastrototaro
20 Gorgonian and Black Coral Assemblages in Deep Coastal
Bottoms and Continental Shelves of the Mediterranean Sea................................ 245
Andrea Gori, Jordi Grinyó, Carlos Dominguez-Carrió, Stefano Ambroso,
Pablo J. López-González, Josep-Maria Gili, Giorgio Bavestrello,
and Marzia Bo
21 Mediterranean Black Coral Communities............................................................. 249
Marzia Bo and Giorgio Bavestrello
22 Recent Discoveries of Extensive Cold-Water Coral Assemblages
in Maltese Waters...................................................................................................... 253
Leyla Knittweis, Julian Evans, Ricardo Aguilar, Helena Álvarez,
Joseph A. Borg, Silvia García, and Patrick J. Schembri
23 Corals of Aphrodite: Dendrophyllia ramea Populations of Cyprus...................... 257
Covadonga Orejas, Carlos Jiménez, Andrea Gori, Jesús Rivera,
Claudio Lo Iacono, Didier Aurelle, Louis Hadjioannou, Antonis Petrou,
and Katerina Achilleos
24 Cold-Water Corals in Fluid Venting Submarine Structures................................. 261
Desirée Palomino, José Luis Rueda, Juan Tomás Vázquez, Javier Urra,
Olga Sánchez-Guillamón, Emilio González-García, Nieves López-González,
and Luis Miguel Fernández-Salas
25 Cold-Water Corals and Mud Volcanoes: Life on a Dynamic Substrate.............. 265
Andres Rüggeberg and Anneleen Foubert
Contents xiii
26 Occurrence of Living Cold-Water Corals at Large Depths Within

Submarine Canyons of the Northwestern Mediterranean Sea............................. 271
Anna Aymà, Jacopo Aguzzi, Miquel Canals, Joan Batista Company,
Galderic Lastras, Ariadna Mecho, and Claudio Lo Iacono
27 Submarine Canyons in the Mediterranean: A Shelter for Cold-Water
Corals......................................................................................................................... 285
Pere Puig and Josep-Maria Gili
28 A Cold-Water Coral Habitat in La Fonera Submarine Canyon,
Northwestern Mediterranean Sea........................................................................... 291
Galderic Lastras, Anna Sanchez-Vidal, and Miquel Canals
29 Cold-Water Coral Associated Fauna in the Mediterranean
Sea and Adjacent Areas............................................................................................ 295
José L. Rueda, Javier Urra, Ricardo Aguilar, Lorenzo Angeletti, Marzia Bo,
Cristina García-Ruiz, Manuel M. González-Duarte, Eduardo López,
Teresa Madurell, Manuel Maldonado, Ángel Mateo-Ramírez, César Megina,
Juan Moreira, Francina Moya, Lais V. Ramalho, Antonietta Rosso, Cèlia Sitjà,
and Marco Taviani
30 Cold-Water Corals as Shelter, Feeding and Life-History Critical
Habitats for Fish Species: Ecological Interactions and Fishing Impact.............. 335
Gianfranco D’Onghia
31 Past, Present and Future Connectivity of Mediterranean Cold-Water
Corals: Patterns, Drivers and Fate in a Technically and Environmentally
Changing World........................................................................................................ 357
Joana Boavida, Ronan Becheler, Anna Maria Addamo, Florent Sylvestre,
and Sophie Arnaud-Haond
32 Desmophyllum dianthus Genetics and More........................................................... 373
Anna Maria Addamo
33 Diversity of Bacteria Associated with the Cold Water Corals
Lophelia pertusa and Madrepora oculata................................................................ 377
Markus G. Weinbauer, Davide Oregioni, Anne Großkurth,
Marie-Emanuelle Kerros, Tilmann Harder, Michael DuBow,
Jean-Pierre Gattuso, and Cornelia Maier
34 Lophelia pertusa and Madrepora oculata: An Archaea Riddle?............................ 387
Markus G. Weinbauer, Davide Oregioni, and Cornelia Maier
35 Biology and Ecophysiology of Mediterranean Cold–Water Corals..................... 391
Stéphanie Reynaud and Christine Ferrier-Pagès
36 Growth Patterns of Mediterranean Calcifying Cold-Water Corals..................... 405
Franck Lartaud, Vincent Mouchi, Leïla Chapron, Anne-Leïla Meistertzheim,
and Nadine Le Bris
37 Demography and Conservation of Deep Corals: The Study
of Population Structure and Dynamics................................................................... 423
Lorenzo Bramanti, Giovanni Santangelo, Maria Carla Benedetti,
Mimmo Iannelli, and Katell Guizien
xiv Contents
38 Cold-Water Coral in Aquaria: Advances and Challenges.

A Focus on the Mediterranean................................................................................ 435
Covadonga Orejas, Marco Taviani, Stefano Ambroso, Vasilis Andreou,
Meri Bilan, Marzia Bo, Sandra Brooke, Paal Buhl-Mortensen, Erik Cordes,
Carlos Dominguez-Carrió, Christine Ferrier-Pagès, Antonio Godinho,
Andrea Gori, Jordi Grinyó, Cristina Gutiérrez-Zárate, Sebastian Hennige,
Carlos Jiménez, Ann I. Larsson, Franck Lartaud, Jay Lunden, Cornelia Maier,
Sandra R. Maier, Juancho Movilla, Fiona Murray, Erwan Peru, Autun Purser,
Maria Rakka, Stéphanie Reynaud, J. Murray Roberts, Pedro Siles,
Susanna M. Strömberg, Laurenz Thomsen, Dick van Oevelen, Alfredo Veiga,
and Marina Carreiro-Silva
39 Approaching Cold-Water Corals to the Society: Novel Ways to Transfer
Knowledge................................................................................................................. 473
Sergio Rossi and Covadonga Orejas
Part III Future
40 Perspectives of Biophysical Modelling with Implications
on Biological Connectivity of Mediterranean Cold-Water Corals....................... 483
Matthew W. Johnston and Ann I. Larsson
41 The Interface Between Tectonic Evolution and Cold-Water
Coral Dynamics in the Mediterranean................................................................... 499
Rinus Wortel and Paul Meijer
42 The Mediterranean Is Getting Saltier: From the Past to the Future................... 507
Nikolaos Skliris
43 The Spread of Non-indigenous Species in the Mediterranean –
A Threat to Cold-Water Corals?............................................................................. 513
Bella S. Galil
44 Fate of Mediterranean Scleractinian Cold-Water Corals
as a Result of Global Climate Change. A Synthesis............................................... 517
Cornelia Maier, Markus G. Weinbauer, and Jean-Pierre Gattuso
45 A Case Study: Variability in the Calcification Response
of Mediterranean Cold-Water Corals to Ocean Acidification.............................. 531
Juancho Movilla
46 Conservation of Cold-Water Corals in the Mediterranean:
Current Status and Future Prospects for Improvement....................................... 535
Maria del Mar Otero and Pilar Marin
Species Index..................................................................................................................... 547
Subject Index..................................................................................................................... 555

Introduction
An Introduction to the Research
on Mediterranean Cold-Water Corals 1
Covadonga Orejas and Carlos Jiménez
1.1 About this Introductory Chapter Despite being separated in three sections (Past, Present
and Future) the sections often contain elements of the other
The aim of this chapter is to introduce the history of the deep- ones. The time-line perspective provides better ecological
sea and specifically living cold-water coral (CWC) research understanding of these deep-sea ecosystems.
in the Mediterranean Sea, as well as additional topics that the
46 chapters included in this volume provide to the marine
researchers interested in this field. The history of CWC 1.2 Discovering the Mediterranean
research in the Mediterranean begun in the eighteenth cen- Deep-Sea Benthos
tury. Several names stand out in the discovery of the
Mediterranean CWCs, but without doubt Jean-Marie Pérès The image of the Mediterranean as a relatively shallow and
has a special place in the tale of the Mediterranean deep living warm-temperate sea still prevails in the collective mind.
coral communities, being one of the pioneers of the However, this picture does not reflect the reality. In the
Mediterranean CWC research. The contributions of Pérès and Mediterranean, deep submarine canyons incise the continen-
others are highlighted in this introductory chapter, as well as tal shelf, reaching depths in excess of 2000 m. Abyssal plains
information about some of the most relevant and pioneering are also present in the central parts of the three main
deep-sea scientific expeditions and marine laboratories. In Mediterranean basins: western, central and eastern. As is the
addition, the main topics of each full and short (“drop”) chap- case for most oceans and seas all over the world, most
ters are succinctly discussed while it is also pointed out that research in the Mediterranean carried out in the past has also
large gaps in the knowledge of Mediterranean CWCs still been focused on the shallow areas. Hence, the story of the
exist (e.g., reproduction, demography). A number of concepts research of the deep parts of the oceans is still young as the
and definitions identified throughout the process of the com- first deep-sea discoveries took place in the middle of the
pilation of this volume were found to respond to multiple nineteenth century (Gage and Tyler 1992). Among the pio-
meanings potentially resulting in confusion within the CWC neer explorers of the life in the deep sea, names such as
research community and thus warranting clarification. In the Michael Sars (1805–1869), Edward Forbes (1815–1854) or
last part of this introductory chapter, a short reflection is Sir Charles Wyville Thomson (1830–1882) stand out. The
included on aspects that we consider need further research Royal Society of London set the foundations of the deep-sea
efforts and discussion, such as the major concern on the future research by supporting the first, truly deep-sea global expe-
of the CWC habitats in the Mediterranean Sea as a result of ditions on board the vessels “Lightning” (1868), the
previous, current and past anthropogenic activities. “Porcupine” (1869, 1870) and the legendary “Challenger”
(1872–1876). At around the same time, Mediterranean
C. Orejas (*) researchers, such as Antoine Risso (1777–1845), described
Instituto Español de Oceanografía (IEO), Centro Oceanográfico de the crustacean and fish faunas at depths from 600 to 1000 m.
Baleares, Palma de Mallorca, Spain These discoveries provided valuable information against the
e-mail: [email protected]
so-called “azoic hypothesis”1 by Forbes (1843). However, at
C. Jiménez
Enalia Physis Environmental Research Centre (ENALIA),
The azoic hypothesis was proposed by Edward Forbes in 1843. It
1
Nicosia, Cyprus
stated that the abundance and variety of marine life decreased with
Energy, Environment and Water Research Centre (EEWRC) increasing depth. By extrapolation of his own measurements, Forbes
of The Cyprus Institute, Nicosia, Cyprus calculated that marine life would cease to exist below 550 m.
© Springer International Publishing AG, part of Springer Nature 2019 3

C. Orejas, C. Jiménez (eds.), Mediterranean Cold-Water Corals: Past, Present and Future, Coral Reefs of the World 9,
https://doi.org/10.1007/978-3-319-91608-8_1
4 C. Orejas and C. Jiménez
the time, these Mediterranean findings were unfortunately nental shelf and by the work on the submarine canyons of the
largely overshadowed by the discoveries from John Ross Gulf of Lions by Reyss (1972–73). To our best knowledge
(1777–1856) and his nephew James Clark Ross (1800–1862) these studies were the first to document the presence of live
from the Antarctic expeditions on board the vessels “Erebus” CWCs in the Mediterranean, reports that came from Cap de
and “Terror” (1839–1843). In 1861, Edward Milne-Edwards Creus (Pérès and Piccard 1964) and Lacaze-Duthiers subma-
(1800–1885) officially rejected the “azoic hypothesis” after rine canyons (Reyss 1964).
the recovery of a damaged submarine cable from >2000 m Corals are normally associated with shallow and warm
depth off Sardinia, which was colonised by dozens of live waters and mostly to the tropical realm. However, CWCs
organisms, mostly molluscs and corals. have been described as early as in the eighteenth century;
Subsequent to these initial discoveries, the Mediterranean some of the first written records are notes by the Right
deep-sea studies were followed by the expedition on board Reverend Erich Pontoppidan, who was the bishop of Bergen
the vessel “Travailleur” (1880–1882), setting off from the in Norway (Pontoppidan 1755, in Roberts et al. 2009). For
Gulf of Biscay in the Atlantic and making its journey to the readers interested in the geology, biology, but also in the his-
western Mediterranean. Later in 1890, the first truly tory of the discovery and research of CWCs, we highly rec-
Mediterranean expedition took place on board the vessel ommend “Cold-water corals. The biology and geology of
“Pola”, and was the first of a series of expeditions across the deep-sea coral habitats” by J. Murray Roberts, Andrew
entire basin. The Prince of Monaco, Albert I, a renowned Wheeler and André Freiwald (2009).
scientist, supported this expedition, which together with the After the pioneer studies, the CWC research in the
creation of the Oceanographic Institute in Paris, as well as Mediterranean proliferated during the 1970s and 1980s. The
the Oceanographic Museum in Monaco, at the beginning of geological and palaeontological aspects were developed
the twentieth century were significant milestones in the his- with remarkable contributions of Marco Taviani, Georgette
tory of marine research in the Mediterranean. Additionally, Delibrias and Philippe Bouchet; the taxonomical research
the research vessels from the Oceanographic Museum in was enriched as a result of the comprehensive work by
Monaco, “Hirondelle I” and “Hirondelle II”, as well as Helmut Zibrowius, and the first attempts to understand CWC
“Princess Alice I” and “Princess Alice II”, were fundamental biogeography. The 1990s marked the beginning of the bio-
for the development of the marine research in the logical studies. These were followed by an exponential
Mediterranean. At the same time, Danish expeditions on increase of ecological and physiological studies on CWCs
board the RV “Thor” and “Dana”, had also the Mediterranean during the first decade of the twenty-first century, for the
as a research target (Mavraki et al. 2016). In mid twentieth most part due to the rapid and important advances in techno-
century, several international scientists played important logical developments and focus on the European deep-water
roles in the Mediterranean basin research, including the ecosystems thanks to large European collaborative projects
deep-sea areas. Among them was Rupert Riedl (1925–2005), (e.g. ACES, HERMES, HERMIONE, CORALFISH). These
who published the most comprehensive guide of the advancements allowed the exploration of great depths in the
Mediterranean flora and fauna (Riedl 1963). Jacques-Yves oceans by means of remotely operated vehicles (ROVs),
Cousteau (1910–1997) is famed for technical advances in the towed cameras, photographic sledges or manned
scuba diving, as well as notable scientific discoveries in the submersibles.
shallow and in the deep-sea Mediterranean by pioneering In this volume, we present the current state of the art in
video recordings of the habitats and for the small submarine Mediterranean CWC research as comprehensively as possi-
known as the “soucoupe plongeante” (diving saucer) that ble. The structure of the book (Past, Present, Future) pro-
opened the gates of information to depths up to -400 m. For vides a “road map” from the paleontological records of
the first time, some of the earliest images of CWC inhabiting CWCs in the Mediterranean, continuing through the
the deep parts of the Mediterranean Sea were shown to research that is currently done in the living CWC communi-
astonished eyes and amazed audiences. While a number of ties inhabiting the basin, culminating in the possible future
scientists largely contributed to increase the knowledge of scenarios awaiting this research. The volume contains two
the deep-sea benthic realm, four in particular are especially different types of contributions, full chapters that are
relevant: Jacques Picard (1922–2008), Jean-Marie Pérès devoted to comprehensive specific topics and reviews, and
(1915–1998), Daniel Desbruyérès and Daniel Reyss. These short chapters (“drops”) consisting of short informative
researchers explored tirelessly the shallows and depths of the essays on recent findings and focus on very specific topics.
Mediterranean. The benthic bionomy of the Mediterranean, A total of 146 authors and approximately 80 reviewers con-
by Pérès and Piccard (1964), is still the most comprehensive tributed in producing the 46 chapters of the present volume.
work closely followed by the one published by Desbruyérès In the following paragraphs we present an overview of these
and collaborators (1972–1973) for the French-Spanish conti- chapters.
1 An Introduction to the Research on Mediterranean Cold-Water Corals 5
1.3 editerranean Cold-Water Corals:

M ronmental conditions and climatic events. However, to obtain
An Old and New Story more accurate interpretations, coral skeleton data should be
related to the current knowledge on coral physiology, includ-
1.3.1 The Old Story ing biomineralisation; this will contribute to a better under-
standing and interpretation of the geochemical proxies.
The information about the Mediterranean CWCs presented Life of any benthic organism is dependent on the currents
here does not refer only to the living communities, but also to surrounding its habitat, and this is also the case for CWCs.
their fossil counterparts. Several chapters highlight the impor- Michele Rebesco and M. Taviani bring together the climate
tant role of the fossil records for the understanding of the past paleo-archives provided by CWCs and the typical
but also of the current state of the Mediterranean CWCs. Mediterranean contourite drifts. The authors explore the
Marco Taviani and co-workers present a short review on effects of the bottom currents as well as the role of contou-
Mediterranean CWC paleoecology, mostly focusing on the rites in the presence of CWCs, highlighting the link between
submerged locations but also considering land occurrences. these geomorphological features and the Levantine
Additionally, in his “drop chapter”, M. Taviani bridges the Intermediate Water (LIW). The LIW seems to be, as it is dis-
past and present through the elaboration of a research timeline cussed in other chapters (Nikolaos Skiris and Daniel Hayes
of the Mediterranean CWCs. In the same context, Julian Evans and co-workers), a key element for the presence of CWCs in
and co-workers highlight in their “drop chapter” the first the Mediterranean basin.
records of Mediterranean CWCs by Carl Linnaeus (1707– For CWCs, the Levantine Basin is one of the regions of
1778), who documented Madrepora oculata. Rare observa- the Mediterranean where not enough research has been con-
tions of living specimens led scientist to believe that the ducted. This is true for both fossil remains and living com-
documented Mediterranean CWC assemblages were relics of munities. Jürgen Titschack presents recent findings on the
the flourishing communities that thrived during the Pleistocene. bathyal coral community in the Aegean Sea including live
As highlighted by M. Taviani, this view has indeed changed and fossil records of CWCs, and gives description of the
only recently with the exploration and discovery of several topographic features and reconstruction of environmental
CWC sites in the western and central Mediterranean basins. conditions in which they were found. Two more
The CWC communities have inhabited the Mediterranean Mediterranean case studies, located in the Alborán Sea are
since at least the Miocene (26–5 million years ago), as dis- presented in the “drop chapters” by Claudia Wienberg and
cussed by Agostina Vertino and co-workers. Their review on by Dierk Hebbeln. Wienberg’s “drop chapter” focus on the
the current state of knowledge on Mediterranean frame- temporal occurrence of CWCs, particularly Lophelia pertusa
building CWCs and solitary species through geological time and M. oculata. These two species formed coral mounds in
is an excellent “sister chapter” of the ones by Giovanni the geological past, experiencing a boom since the last degla-
Chimienti and co-workers and José Luis Rueda and co- ciation until the Early Holocene (~10,000 years ago). During
workers. They describe, respectively, the current bio- this period, a shift in coral species dominance took place
geographic distribution of the living CWC communities and with M. oculata-dominated CWC communities in the
present day Mediterranean CWCs fauna. Throughout their Mediterranean. The author hypothesised that the higher tem-
history, environmental fluctuations and catastrophic events perature tolerance of M. oculata for warmer waters was one
took place affecting the occurrence and distribution of the of the most important factors for such shift in dominance.
CWC communities in the Mediterranean. André Freiwald Hebbeln describe the impressive seafloor structures formed
revised in his “drop chapter” one of the fundamental events by CWCs from East Melilla CWC Mound Province with
that occurred in the Mediterranean during the Late Miocene: highly variable morphologies and dimensions, discussing the
the Messinian Salinity Crisis. The author gives a brief descrip- different drivers which might have interacted to generate
tion of CWC communities before, during and after this major these astonishing seascapes.
event. A. Vertino and Cesare Corselli highlight in their “drop The history described through the chapters dealing with
chapter” the ability of CWC to store historically important the “old” story is fundamental for the understanding of the
climatic information and use fossil records of Mediterranean past of CWCs, but also for the understanding of today’s state
deep-sea corals to demonstrate the strength of the influence of of the Mediterranean CWC communities.
climatic variations on the distribution and diversity of CWCs
during the Quaternary (1.6–0.01 millions of years ago). The
importance of fossil CWCs as climatic archives is compre- 1.3.2 The New Story
hensively discussed by Paolo Montagna and M. Taviani. By
storing information about the changing physico-chemical The study of the living CWCs of the Mediterranean is still in
properties of the surrounding seawater within their aragonite its infancy and many research fields are yet to be explored
skeleton, scleractinian CWCs can shed light on the past envi- and developed. A basic and fundamental aspect when under-
taking the study of any living organism is the taxonomy; vent subsequent misrepresentations of the real meaning of the
without taxonomic knowledge the study of the biological word “province” in the biogeographical context. The term
and ecological characteristics of the species will be meaning- “province” was originally coined within the botanical sci-
less. In their comprehensive overview of the taxonomy of the ence, and the definitions included in the Dictionary of
Mediterranean CWCs, Álvaro Altuna and Angelo Poliseno Ecology, Evolution and Systematics by Lincoln et al. (1998)
include species of the six orders of the phylum Cnidaria are: “…1. A major division of the biosphere; 2. A phytogeo-
(Antipatharia, Scleractinia, Zoantharia, Alcyonacea, graphical subdivision of a region characterised by dominant
Pennatulacea and Anthoathecata) totalling 82 species of plant species of similar past history; 3. A biogeographical
deep-sea corals, 13 of which with habitat-building ability at zone characterised by a 25–50 percent endemic flora or
depths of 200 m and below. fauna.” Pondering these original definitions, it is worthy to
The reader might have realised that in the previous sen- recall for some specifications when using the term “province”
tence the term “deep-sea corals” was used instead of “CWCs”, in the case of the CWCs. While the definition of “province” in
which is the term most frequently used to refer to this group the biogeographical context considers large spatial scales,
of organisms. This is something we would like to briefly currently studied areas with CWCs in the Mediterranean
address at this point of this introductory chapter. Through the exhibit notably smaller spatial extension. Therefore, further
process of compiling the contributions for this volume, it was discussions are needed when using the term “CWC province”
recognised that certain concepts and topics were poorly which would take into consideration aspects like spatial scale,
defined or unclear, resulting thus in slightly, and on occasion dimensions or even distribution patterns of CWCs, in order to
strikingly, different interpretations between the various chap- distinguish this “province” to the original definition in the
ters. These emerging issues are not necessarily a problem, biogeographical context.
they can be considered as an interesting and stimulating part Generally, most studies on CWCs have been focused on
of the scientific discussion, flagging the need to revisit some scleractinian corals, remarkably the so-called “coral triad”
concepts and definitions. This is the case for “CWC” or (Pérès and Piccard 1964): L. pertusa, M. oculata and
“deep-sea coral” concepts. Some authors considered both Desmophyllum dianthus. However, there are other groups,
terms as synonyms. Others were, however, inclined to use such as octocorals and antipatharians, which are also eco-
“deep-sea corals” for the specific case of the Mediterranean logically important, forming dense populations and dominat-
Sea due to the fact that the temperatures of the Mediterranean ing benthic communities. Two “drop chapters” are dedicated
deep-sea areas rarely decrease below 12–13 °C. Altuna and to the gorgonian and black coral assemblages found in the
Poliseno dedicated a specific section in their chapter to this deep Mediterranean. Andrea Gori and co-workers present an
issue, presenting the different concepts according to different overview on recent studies investigating the gorgonian and
authors, when using the term CWC. Altuna and Poliseno’s black coral communities inhabiting the deep coastal seafloor
chapter was exclusively based on corals occurring below and continental shelves, mostly of the western and central
50 m depth, regardless of whether they are habitat builders or Mediterranean, whereas Marzia Bo and Giorgio Bavestrello
not. In contrast, other authors (e.g. G. Chimienti and co- summarise some of the most recent findings, such as the fun-
workers) used the concept of CWC only when dealing with damental role these coral gardens play as structuring com-
framework-building species. The chapter by Chimienti and munities. Advances in taxonomical knowledge and
co-workers presents a comprehensive review of the current discoveries of new populations and communities also con-
knowledge of the occurrence and biogeography of CWCs tribute to increasing information of the CWC biogeography,
across the Mediterranean basin, in the context of oceanogra- which is fundamental for generation and improvement of the
phy, bottom topography, geographical areas of distribution, as mapping of habitats populated by these deep-sea communi-
well as the bathymetric ranges. The biogeographical approach ties. In the chapter by Claudio Lo Iacono and co-workers,
of these authors is partially based in the “CWC- province” two of the most researched CWC areas of the Mediterranean
concept. The term “province” in the context of CWC studies are revisited: the Chella Bank (also known as Seco de los
was firstly used in publications from the Atlantic Ocean (e.g., Olivos) in the Alborán Sea, and the CWC province of Santa
Henriet et al. 1998) as “deep-water reef provinces” or “mound Maria di Leuca in the Ionian Sea. The authors present a com-
province”, and later from the Mediterranean as “CWC prov- prehensive and integrated study of the environmental charac-
ince” by Taviani et al. (2011). The difference in interpretation teristics of the benthic habitats. To identify the geological
of the “CWC province” concept that appears in the chapters and oceanographic processes, most likely responsible for the
of this volume gives foundation for further interesting and CWC distribution and associated benthic communities, habi-
stimulating scientific discussions among researchers, which tat mapping is performed using supervised automated clas-
we believe deserve additional attention and perhaps also a re- sifications, applying a combination of several methodological
formulation and redefinition of the concept. This might pre- approaches.
Several of the submarine canyons explored in the the readers will realise that some fundamental aspects have
Mediterranean are characterised by conditions suitable for not been included. This is the case of reproductive and larval
settlement and development of CWCs. La Fonera and Blanes biology and ecology. To the best of our knowledge, there is
canyons are discussed in the chapter by Anna Aymà and co- not a single publication dealing with this topic for
workers; they describe CWC habitats in the canyons with Mediterranean CWCs. However, this important aspect is
different dominance of the species, including novel, deep summarised by S. Reynaud and C. Ferrier-Pagès, who
records in the Mediterranean for D. dianthus, documented in reviewed literature mostly available for the North Atlantic.
La Fonera as deep as 1400 m. Further details about La Fonera Franck Lartaud and co-workers reviewed the studies on the
are given by Galderic Lastras and co-workers in their “drop most important aspects of coral growth processes: from skel-
chapter”. The authors describe the features of the communi- eton microstructure and crystallography to the different
ties dominated by M. oculata, as well as the results on pre- methodologies applied to measure and study CWC growth.
dictive habitat modelling, showing the extent of the CWC The growth process is also discussed at different scales, from
habitats in this canyon. Cap de Creus canyon, located in the colony to reef formation, where environmental factors and
Gulf of Lions, is reviewed in the “drop chapter” by Pere Puig their influence on present and future growth scenarios were
and Josep Maria Gili, complementing the information given considered.
in the other canyon-themed. The authors present a short Closely related to reproduction processes and growth is
overview of the northwestern Mediterranean canyons, where the demography of CWC populations. To the best of our
the first CWCs in the Mediterranean were reported. knowledge, only scarce literature on this subject is available
Other topographic features in the Mediterranean Sea (but see Gori et al. 2013) worldwide. Lorenzo Bramanti and
where CWC are known to exist are the fluid-venting subma- co-workers provide an introduction to the science of demog-
rine structures. Two “drop chapters” describe different raphy, which originated long time ago for the purpose of tax
aspects of the vents. Desirée Palomino and co-workers high- collection and conscription orders. From these origins to ani-
light the role of mud volcanoes and mud diapirs as habitats mal demography, the review encompasses different method-
for CWCs. Additionally, they describe the typical fauna ologies, models and the results for one of the most well
associated with these features in several Mediterranean loca- studied species in the Mediterranean, the precious red coral
tions and briefly summarise the formation processes of these (Corallium rubrum). Although this gorgonian, considered as
features. Andres Rüggeberg and Anneleen Foubert focus on quasi-endemic from the Mediterranean, is not a CWC sensu
the origin and the past history of these features, including stricto, the species reach very great depths and has been
fossil records, describing the different records of these fluid recorded down to 1016 m (Knittweis et al. 2016). The lack of
venting submarine structures in the Mediterranean. demographic models for CWCs in the Mediterranean and
Although the Mediterranean deep-sea is still a largely elsewhere, is identified as one of the aspects (together with
unexplored realm, the increasing number of explorations reproduction and larval studies) that needs to be urgently
owed to current technological developments, is notable. Some addressed in the incoming research.
of the recently explored deep-sea areas reveal new CWC Although the collection of contributions in this volume
sites, which are described in several contributions. Leyla clearly reveal the important advances made in CWC research
Knittweiss and co-workers present the recently discovered during recent decades, generally, and in the Mediterranean in
CWCs in Maltese waters and Covadonga Orejas and co- particular, society is still unaware of the existence of these
workers demonstrate the recent discovery of a Dendrophyllia spectacular deep-sea communities. Efforts must be made
ramea population off Cyprus at about 150 m depth. from the scientific side, to transfer knowledge to the general
The advances in the biological, physiological and eco- public; reflective thoughts on this topic are presented by
logical fields of Mediterranean CWC species, communities Sergio Rossi and Covadonga Orejas in a “drop chapter”.
and habitats are presented in an updated and comprehensive
manner in several of the chapters. Biology and physiology of
scleractinian CWCs are reviewed by Stéphanie Reynaud and 1.4 old-Water Coral Structure, Shelter,
C
Christine Ferrier-Pagès. These authors compare the responses and Associated Diversity
of CWCs to changes of environmental parameters; they con-
sider feeding rates and preferences, respiration, and the role Bioengineering species (sensu Jones et al. 1994), such as
of these organisms in the organic matter fluxes. Knowledge CWCs, modify the environment they inhabit, and those
on the biological traits and functionality of the species is fun- places are widely recognised and documented as biodiversity
damental for ecological studies, and to be able to develop hotspots (e.g., Henry and Roberts 2016). The Mediterranean
and apply management and conservation measures. However, is not an exception; CWC ecosystems have been comprehen-
many basic aspects of the CWC biology in the Mediterranean sively studied and have a high diversity of associated spe-
are still unknown. This fact is also reflected in this book and cies, from invertebrates to vertebrates (fish), many of which
are of commercial interest. In the chapter by José Luis Rueda changes which are experienced due to the tectonic activity.
and co-workers, an historical background of studies dealing The authors discuss the potential effects of those changes on
with CWC associated diversity is presented. It includes a the CWC habitats, as well as revisiting their past history and
comprehensive, up-to-date, and illustrated comparative (with current evolution. Thus, this complements the discussions
the Atlantic Ocean) overview on the high diversity of associ- regarding the connectivity of water masses and their effects
ated species of different CWC communities across the on CWC ecosystems given in other chapters, such as in the
Mediterranean Sea. The chapter is structured in subchapters one by Joana Boavida and co-workers and in the “drop chap-
according to different taxa: Porifera, Cnidaria, Annellida, ter” by Bella Galil.
Mollusc, Crustacea, Echinodermata, Bryozoa, Brachiopoda, Finally, the increasing evaporation in the Mediterranean
Teleostea and Chondrichthya. The last two taxa are also dis- Sea, together with the decrease of freshwater river discharge
cussed in the chapter by Gianfranco D’Onghia. The leading to a higher net evaporation in the Mediterranean, is
Mediterranean CWC communities’ role as Essential Fish discussed by Nikolaos Skliris reviewing the effects of such a
Habitat (EFH) is highlighted, as well as their fundamental strong evaporation on the salinity from the surface to the
function as shelter, feeding and life-history critical habitat deep layers of the sea, influencing the LIW and consequently,
for many fish species including several of commercial the occurrence and distribution of CWC habitats.
importance.
The biodiversity hotspot role played by CWC communi-
ties not only refers to metazoans but also to microorganisms. 1.6 Understanding Distribution Patterns
This is still an unexplored world; Markus Weinbauer and co- and the Mediterranean – Atlantic Link:
workers, review this research in the Mediterranean, and pres- Studies on Connectivity
ent the bacterial diversity and biogeography associated to
Lophelia pertusa and Madrepora oculata. In another “drop The geographical distribution of CWC species is linked to
chapter”, Weinbauer and co-workers deal with a specific many factors; while some are environmental (e.g. suitability
topic in the same context: the potential role of Archaea in the of the habitat, parameters of the water column), others are
specific case of CWCs, as high abundance of Archaea in the intrinsic to the biological characteristics of the species. An
abiotic and biotic environment of CWCs is detected. example of the latter is the dispersal capability of the coral
larvae, which together with the oceanographic patterns of the
area, will be crucial to allow the dispersion of coral propa-
1.5 old-Water Corals, Oceanographic
C gules at short or large distances. The small size of planulae
and Geological Past, Present and the large dimensions of the oceans and seas make track-
and Future ing of coral larva virtually impossible. Fortunately molecular
analyses provide the means to estimate connectivity between
Life in the oceans cannot be understood without taking into populations at different spatial and/or temporal scales.
account the oceanographic features, which embed pelagic Boavida and co-workers review the new insights and meth-
ecosystems and surround the benthic ones. The CWC com- odologies dealing with the genetic dispersion patterns of
munities are not an exception; the understanding of the CWCs in the Mediterranean. They also review the present
occurrence of these communities in specific locations is knowledge on this research field and highlight the studies
directly related to the water circulation regimes of these dealing with the connectivity between the Atlantic Ocean
areas, which in turn, directly affect the transport and delivery and the Mediterranean Sea. Related to this review topic,
of food to these organisms and their associated fauna. Daniel Anna Maria Addamo presents a specific case study that
Hayes and co-workers describe the main features of the cir- focuses on Desmophyllum dianthus, summarising the most
culation and properties of the intermediate water masses of recent and novel information on the molecular ecology, sys-
the Mediterranean. The authors review the paramount impor- tematics and evolution of this CWC species. There are still
tance that the LIW seems to play for the presence of many pieces to gather of the complicated Mediterranean
Mediterranean CWC communities, which is also discussed CWCs connectivity puzzle. Indeed, as previously mentioned,
by M. Taviani and J. Evans and co-workers in two “drop basic aspects such as reproductive traits have not being stud-
chapters”, among others. Two other contributions deal with ied for Mediterranean CWC species. The environmental con-
specific aspects of the circulation patterns in the ditions are fundamental when tackling the study of species
Mediterranean and their effects on the CWC habitats. One of connectivity. The contribution of Matthew Johnston and Ann
the main characteristics of the Mediterranean is the connec- Larsson brings together both the oceanographic expertise
tion to other water masses, notably the Atlantic Ocean, but and the knowledge on CWC dispersion; this chapter com-
also to the Black and the Red Seas. Rinus Wortel and Paul bines the current knowledge on Mediterranean oceano-
Meijer discuss the importance of these connections and the graphic patterns and the existing knowledge on CWC
planulae. This topic has been mostly developed in the NE the deep sea. However, some experimental work, using
Atlantic, at the large reefs built by Lophelia pertusa off the ROVs has been done: stained corals were deployed to study
Norwegian margin. in situ growth rates of the corals (see chapter by F. Lartaud
and co-workers). The caveat of this type of experimental
work on CWCs is that it often needs to take place ex situ in
1.7 Approaching the Study research centres, universities or aquaria with suitable facili-
of the Mediterranean Cold-Water ties and systems. Several chapters discuss the results of
Corals at Different Scales experiments conducted in aquaria equipped with the proper
infrastructure (e.g. S. Reynaud and C. Ferrier-Pagès,
An important aspect included in this volume is the current F. Lartaud and co-workers, among others). The contribution
state of methodological approaches developed to study by Covadonga Orejas and co-workers aims to be a practical
Mediterranean CWC communities. Methodologies vary guide/handbook on CWC aquaria research, providing many
according to studies: from paleo research to models gener- examples from aquaria facilities working with Mediterranean
ated to predict future scenarios, as well as methodological and word wide CWCs.
approaches that deal with different physical and temporal
scales included in the book. Lorenzo Angeletti and co-
workers discuss the use of X-ray Computed Tomography as 1.8 hreats for Cold-Water Corals
T
a useful, non-destructive technique to detect the presence, in the Mediterranean Sea, Conservation
content and preservation of CWCs in sedimentary cores, Actions and Perspectives
facilitating taxonomic identification, recognition of the coral
three-dimensional distribution as well as taphonomic aspects. The fate of Mediterranean CWC communities is inexorably
Within the study of the occurrence and distribution of any linked to environmental and biological factors, as well as to
CWC species mapping is a fundamental aspect – mentioned the anthropogenic activities conducted directly in the coral
earlier when commenting the contribution of C. Lo Iacono habitats and/or within their vicinity. The decrease of marine
and co-workers. Mapping is an important approach for any resources in shallow waters, due to overfishing, has led to an
biogeographical and taxonomic study, especially for biologi- increased depth range in which the fisheries sector operates,
cal and ecological studies as species can display different reaching the deep benthic ecosystems where CWCs thrive.
adaptations/accommodations depending on the past and To identify and quantify the threats affecting Mediterranean
present distribution ranges. The chapter by L. Angeletti and CWCs is a key step to find solutions and develop strategies
co-workers is fully dedicated to the multiscale habitat map- for proper conservation of these precious habitats, and for
ping and the up-to-date technologies devoted to this aim, sustainable management of the deep-sea fisheries resources.
utilising Mediterranean examples of CWCs. It is important to remember that many Mediterranean CWC
There is no doubt that image technologies are the most habitats have been identified as fundamental for the develop-
important recent contributions to approach the study of the mental stages of invertebrates and fish, acting as a nursery
deep-sea benthic ecosystems in a non-destructive way. The for species, many of which are of significant commercial
possibility to visualise, count and measure organisms, thanks interest. The CWC habitats also constitute feeding grounds
to georeferenced video recording and the use of scaling ele- or refuge for many species, a topic that is discussed in
ments (e.g. laser pointers), highly increases the possibilities G. D’Onghia’s chapter. A comprehensive review on the
of video footage to be considered among the essential ele- threats to CWCs as well as the current situation of the con-
ments in scientific research. Several chapters in this collec- servation of these ecosystems is presented by Maria del Mar
tive volume (e.g. A. Gori and co-workers, M. Bo and Otero and Pilar Marin. The authors also highlight new per-
G. Bavestrello, L. Knittweiss and co-workers, among many spectives to improve the conservation of these hidden habi-
others), present results obtained with underwater cameras. tats. Besides the direct and mechanical effects of fisheries,
Maia Fourt and co-workers deals with the visual method- which is unquestionably the most important impact currently
ological approach and its application in some deep-sea areas affecting Mediterranean CWCs, there are also the indirect
in France, specifically the Mediterranean submarine canyons effects of the anthropogenic activities. Global change is now
of the Gulf of Lions. widely accepted as a fact; the most conspicuous and well-
Besides the in situ and non-destructive approach of video studied effects of global change are warming and ocean acid-
and photographic cameras, there is a fundamental method- ification (OA), with most research conducted in shallow
ological issue when talking about developing experimental water environments. During the last two decades, similar
work at the organism level in deep-sea areas. In tropical and studies emerged from the deep-sea realm and most specifi-
temperate shallow areas, in situ experimental work is usually cally, from CWC communities’ research. In this volume, two
feasible using SCUBA equipment which is not feasible in contributions deal exclusively with the effects of global
change on Mediterranean CWCs. Cornelia Maier and co- are confident that long-term submarine observatories can be
workers review the Mediterranean CWC research on warm- deployed in the Mediterranean in the near future. Among the
ing and OA offering also comparisons with results obtained processes, which are still insufficiently investigated globally,
in other areas, whereas Juancho Movilla offers a specific is the role of the CWC ecosystems in the geochemical fluxes
case study focused primarily on the effects of OA in the cal- and carbon cycling. Recently, this gap has also been high-
cification response of four Mediterranean CWC species. lighted for other benthic ecosystems dominated by animals
Additionally, S. Reynaud and C. Ferrier-Pagès also highlight (Rossi et al. 2017). One of the few works conducted on this
the effects of global change on Mediterranean CWCs. field in the NE Atlantic revealed that coral communities are
One of the consequences of global change is the spread of hotspots of biomass and carbon cycling along continental
non-indigenous species, that is now widely studied in margins (van Oevelen et al. 2009). We hope that an increas-
Mediterranean shallow waters. Utilising previous findings ing number of projects in the Mediterranean will contribute
and experiences from the Caribbean, Bella Galil tackles the to enhance our knowledge on the functionality of these deep-
potential effects of non-indigenous species in Mediterranean sea ecosystems in this semi-enclosed sea.
mesophotic and CWC communities, based on the increasing Holistic and seasonal sampling of the deep-sea
depth range colonised by non-indigenous species arriving to Mediterranean ecosystems is also needed to better under-
the Mediterranean through the Suez Canal. The expansion of stand the environmental characteristics of CWCs’ surround-
these species is expected to increase due to global change. ings, among others, to obtain insights into the Mediterranean
CWC trophic ecology. Although several aquaria experiments
have already been conducted with CWCs, as well as various
1.9 …Still Much Work to Do studies using stable isotopes (see Carlier et al. 2009; Tsounis
et al. 2010; Gori et al. 2015), we still lack sufficient informa-
Rapid advances in the research on CWCs in the last two tion on the composition of the potential food available in the
decades guarantee new discoveries and promise exponen- Mediterranean deep-sea, including differences among the
tially increasing knowledge. Certainly, this knowledge will seasons and the potential selectivity of corals for certain prey
come with the technological progress made in underwater items.
equipment; however, it also depends on the willingness of With regards to other ecophysiological aspects of the
governments to finance deep-sea research. Mediterranean CWCs, S. Reynaud and C. Ferrier-Pagès also
As previously mentioned, to date, reproduction studies on stress in their chapter the need to gain more knowledge on
Mediterranean CWC species are completely lacking. The calcification processes. The current knowledge indicates
results available from the Atlantic revealed differences in very different calcification rates obtained for the same spe-
reproductive timing for different geographical regions (e.g., cies under different environmental conditions. The fact that
Waller and Tyler 2005; Brooke and Jarnegren 2013). The calcification may also vary with the polyp age demonstrates
studies on reproductive traits of Mediterranean CWCs could the need to better understand the influence of the different
contribute with further information concerning the reproduc- factors and their synergies on the calcification process. One
tive timing, but also the potential influence on CWC repro- of the environmental stressors which has already been inves-
duction of environmental parameters which are specific for tigated in Mediterranean CWC communities is OA, and sev-
this sea. In species with Atlanto-Mediterranean distribution, eral works (see C. Maier and co-workers in this volume and
such as the ubiquitous Lophelia pertusa, knowledge on lar- references therein) revealed the synergic effects of OA and
val features could also reveal potential differences between temperature. However, in view of the increasing anthropo-
conspecifics of both seas. Closely linked to reproductive pro- genic activities and their impacts on deep-sea ecosystems,
cesses and traits are demographic studies. The chapter on studies combining different stressors and its effects on the
this topic reveals the almost complete ignorance that exists CWC Mediterranean ecosystems are highly necessary. For
concerning information on CWC population dynamics. It instance, local impacts such as high sedimentation levels,
further indicates the need for advances in dating and repro- which are linked to bottom trawling, drilling and mining
duction studies as well as in software tools to improve the activities, should be studied in combination with impacts
processing of underwater videos – this could enhance the acting globally or regionally, such as thermal stress or high
knowledge on this issue. Another useful approach to obtain pCO2.
valuable information would be a continuous monitoring of Several chapters in this volume revealed that studies on
deep-sea ecosystems; an expensive and challenging biodiversity have mostly been conducted in the central
approach, although some pioneering examples in the North Mediterranean (see for instance J.L. Rueda and co-workers);
Atlantic and Pacific Oceans are highly promising. This meth- which highlights the need to investigate CWC associated
odological approach is considered to be fundamental for the fauna in the Mediterranean, notably in the Levantine, and in
understanding of the dynamics of these ecosystems and we general in the southern part of the Mediterranean basin.
Furthermore, available biodiversity studies are mostly it is our duty to give our feedback to the general public.
focused on the megabenthic organisms. Two chapters by Finding the right approaches, words and language to reach
Markus Weinbauer and co-workers are dedicated to the people is fundamental to demonstrate the vital role that these
microbial communities associated to Mediterranean CWCs. hidden ecosystems play in the oceans and thus, their impor-
Both chapters highlight the scarce number of studies con- tance and value for us, mankind.
ducted on microbial communities to date, although available On a final note, a few days before going to press, a taxo-
information indicate their very important role in ecosystem nomic change occurred of the emblematic white coral
functionality, as recently discovered in the “sponge loop” (de Lophelia pertusa; the accepted name by WoRMS is now
Goeij et al. 2013). Even other associated diversity is com- Desmophyllum pertusum (Linnaeus 1758).2 Due to time con-
pletely understudied as it is the case for symbiotic relation- strains, it was decided to maintain the former in all sections
ships, such as mutualism or parasitism in Mediterranean of the book.
CWCs. Apart from the well-known symbiosis-like relation-
ship between L. pertusa and Eunice norvegica (Mueller et al. Acknowledgements We are in debt with Claudia Wienberg, Andrea
2013), and some studies conducted in the Norwegian fjords Gori and Wolf Isbert for their critical view and constructive comments
to earlier versions of this manuscript. Many thanks also to Cruz Iglesias
on symbiotic relationships with associated fauna (see Buhl- for her constant help in finding old books and hidden documents of the
Mortensen and Buhl- Mortensen 2005), to the best of our first steps in Mediterranean deep-sea research. The authors are highly
knowledge, no works have been published on these topics for grateful to all contributors of this volume. Last but not least we are in
Mediterranean CWCs. debt with Adam Gouragine and Heather Baxter who carefully read the
chapter and highly improved the English of the original manuscript.
The reader will realise that the “Future” section of the This project has received funding from the European Union’s Horizon
book contains fewer chapters than the “Past” and “Present” 2020 research and innovation programme under grant agreement No
sections, which reflects the low numbers of studies con- 678760 (ATLAS). This output reflects only the author’s view and the
ducted in predictive models regarding CWC ecosystems. European Union cannot be held responsible for any use that may be
made of the information contained therein.
This is also partially attributable to the Mediterranean CWC
research where this topic is still in its infancy. To the best of
our knowledge, the publication of the first paper on predic-
tive habitat mapping for Mediterranean CWC (Lo Iacono References
et al. 2018) coincides with the completion of this volume.
The chapter by C. Lo Iacono and co-workers presents predic- Brooke S, Jarnegren J (2013) Reproductive periodicity of the sclerac-
tinian coral Lophelia pertusa from the Trondheim Fjord, Norway.
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lata in the Cap de Creus canyon (NW Mediterranean). Future Buhl-Mortensen L, Buhl- Mortensen P (2005) Distribution and diver-
basic research will allow the addition of new data to feed sity of species associated with deep-sea gorgonian corals off
predictive models, not only with regard to habitat suitability, Atlantic Canada. In: Freiwald A, Roberts JM (eds) Cold-water cor-
als and ecosystems. Springer, Berlin, Heidelberg, pp 849–879
but also considering future climate scenarios such as the Carlier A, Le Guilloux E, Olu K, et al (2009) Trophic relationships in a
ones from the Intergovernmental Panel on Climate Change deep Mediterranean cold-water coral bank (Santa Maria di Leuca,
(IPCC). Additionally, further information on species distri- Ionian Sea). Mar Ecol Progr Ser 397:125–137
bution will also enable the performance of species distribu- de Goeij JM, van Oevelen D, Vermeij MJ, et al (2013) Surviving in a
marine desert: the sponge loop retains resources within coral reefs.
tion models (SDMs) in Mediterranean CWC ecosystems. Science 342:108–110
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Part I
Past
Paleoecology of Mediterranean
Cold-Water Corals 2
Marco Taviani, Agostina Vertino, Lorenzo Angeletti,
Paolo Montagna, and Alessandro Remia
Abstract Keywords
Atlantic-type scleractinian cold-water corals occur in the Cold-water coral · Mediterranean basin · Fossil ·
Quaternary of the Mediterranean basin. Most fossil evi- Taphonomy · Paleoecology
dence on-land is Early Pleistocene in age, and occurs in
peninsular Italy, Sicily and on some Greek islands, whilst
submerged situations are by large late Pleistocene. 2.1 Introduction
According to circumstances, the mode of preservation of
fossil cold-water coral varies sensibly (from loose corals Understanding the spatio-temporal distribution and function-
to micritic limestones) what affects the level of confi- ing of corals inhabiting deep waters is currently a central
dence of the paleoecological reconstruction. All known issue in science because of their value as biodiversity
situations point about a bathyal setting for such cold- hotspots, ecosystemic services and paleoclimatic potential
water coral hosting deposits in the Mediterranean basin, (Freiwald et al. 2004; Roberts et al. 2006; Armstrong et al.
but under many respects the geological record of cold- 2014; Robinson et al. 2014; Henry and Roberts 2017;
water coral paleoenvironments is yet largely under- Montagna and Taviani, this volume). These corals are col-
worked. Research developments are discussed, with spe- lectively recognised in the literature under the name of deep-
cial emphasis on the widespread submarine occurrences (DWC) or cold-water (CWC) corals. Both definitions are
which prevail over the on-land cold-water coral legacy. somewhat ambiguous, however. Although most such corals
are, in fact, established at bathyal depths >200 m, on peculiar
situations like fjords they can be found at very shallow
M. Taviani
Institute of Marine Sciences (ISMAR-CNR), Bologna, Italy bathymetries (Rapp and Sneli, 1999; Försterra et al. 2005;
Järnegren and Kutti 2014). On the other hand, these corals
Biology Department, Woods Hole Oceanographic Institution,
Woods Hole, MA, USA are distributed in a temperature range of 4°–14 °C (Freiwald
et al. 2009; Roberts et al. 2009) up to 21 °C in the Red Sea
Stazione Zoologica Anton Dohrn, Naples, Italy
(Qurban et al. 2014), what makes the term ‘cold’ question-
A. Vertino
able. ‘Corals’ include cnidarians equipped with mineralised
CONISMA Local Research Unit (LRU) of Milano-Bicocca,
Department of Earth and Environmental Sciences, Milano-Bicocca or proteinaceous skeletal parts (Cairns 2007). Conventionally,
University, Milan, Italy here we adopt CWC, the term currently enjoying a general
Department of Geology, Renard Centre of Marine Geology, Ghent acceptance, and restrict our discussion to the sole Scleractinia.
University, Ghent, Belgium Scleractinians are cnidarians provided with an aragonitic
L. Angeletti · A. Remia (*) skeleton prone to be fossilised. Comparatively little is pub-
Institute of Marine Sciences (ISMAR-CNR), Bologna, Italy lished on the paleoecological reconstruction of former CWC
e-mail: [email protected] environments. As documented by their modern distribution,
P. Montagna CWC display a rather patchy distribution in the ocean set-
Institute of Marine Sciences (ISMAR-CNR), Bologna, Italy tling preferentially hard substrates at bathyal depths
Laboratoire des Sciences du Climat et de l’Environnement LSCE/ (Freiwald et al. 2004; Roberts et al. 2006), what partly
IPSL, CEA-CNRS-UVSQ, Université Paris-Saclay, explains why their overall geological record is scanter than
Gif-sur-Yvette, France
their shallow water counterparts (Cairns and Stanley Jr 1981;
Lamont-Doherty Earth Observatory, Columbia University, Stanley Jr and Cairns 1988; Roberts et al. 2009).
Palisades, NY, USA

https://doi.org/10.1007/978-3-319-91608-8_2
16 M. Taviani et al.
Fossil extant-type CWC habitats are, in fact, best exposed The main architects of extant Mediterranean CWC bio-
in contexts where propitious geological situations drive to constructions are the branching scleractinians L. pertusa and
the uplift of deep-water sediments like compressive scenar- M. oculata. The solitary but often gregarious up to pseudoco-
ios in the Mediterranean or New Zealand (e.g., Squires 1964; lonial scleractinian Desmophyllum dianthus, genetically
Vella 1964; Beu and Climo 1974; Wells 1986; Barrier et al. almost indistinguishable from the truly colonial L. pertusa
1992; Freiwald 2002; Taviani et al. 2005a, b; Titschack and (Addamo et al. 2016), may contribute substantially to deep-
Freiwald 2005; Roberts et al. 2009; Vertino et al. 2014, this water coral bioconstructions. Other scleractinians such as
volume, with references therein). Stenocyathus vermiformis, Javania cailleti, Caryophyllia
Submarine Quaternary CWC are instead relatively com- spp., and Dendrophyllia cornigera often participate to CWC
mon in the ocean (e.g., Ayers and Pilkey 1981; Newton et al. habitats (Freiwald et al. 2009; Vertino et al. 2010; Angeletti
1987; Taviani et al. 1991, 2007; Wilber and Neumann 1993; et al. 2014; Chimienti et al., this volume; Rueda et al., this
Adkins et al. 1998; Frank et al. 2004, 2011a, b; Schröder- volume; Vertino et al., this volume).
Ritzrau et al. 2005; Ross and Nizinski 2007; Wienberg et al. A variety of other skeletonised invertebrates, therefore in
2009, 2018; Thresher et al. 2011; Douarin et al. 2013). Their principle easily fossilisable, co-occurs with the main CWC
preservation ranges from pristine to intensely degraded and frame builders among which other cnidarians (calcitic octo-
bioeroded (Freiwald and Schönfeld 1996; Freiwald and corals), molluscs, barnacles, brachiopods, serpulids etc.
Wilson 1998; Freiwald et al. 2002; Wisshak et al. 2005; (Remia and Taviani 2005; Zibrowius and Taviani 2005;
Beuck et al. 2007, 2010; Henry and Roberts 2017). Taviani et al. 2009, 2011a; Mastrototaro et al. 2010; Rosso
Patination by Fe-Mn-oxides is common place whenever et al. 2010; Sanfilippo et al. 2013; Sartoretto and Zibrowius
CWC got prolonged exposure to seawater (e.g., Mullins 2017; Nasto et al. 2018; Rueda et al., this volume).
et al. 1981; Wilber and Neumann 1993; Taviani 1998; The occurrence in the Mediterranean basin of extant
Taviani et al. 2011a). These CWC can even concur to the frame-builders CWC since the Miocene at least has been
formation of large to giant coral mounds from the Pliocene reported in the literature (Taviani et al. 2005a, b; Vertino
onwards (van Weering et al. 2003; Dorschel et al. 2005; et al. 2014). Here we take into consideration only the post-
Ferdelman et al. 2006a; Kano et al. 2007; Wheeler et al. Messinian history as the starting point of the renewed
2007; Eisele et al. 2008; Comas et al. 2009; Foubert and Mediterranean benthic biota (Corselli 2001; Taviani 2003;
Henriet 2009; Frank et al. 2009; Thierens et al. 2009, 2013; Sabelli and Taviani 2014; Freiwald, this volume).
Wienberg et al. 2010a, b; Henriet et al. 2011; Douarin et al. The present chapter briefly reviews examples recorded in
2013; Lo Iacono et al. 2014; Raddatz et al. 2014; Wienberg the literature regarding the paleoecology of Mediterranean
and Titschack 2017). scleractinian CWC (Fig. 2.1) with emphasis on the sub-
Because of its geodynamic evolution, the Mediterranean merged occurrences, and provides hints on current and future
basin is a key-area of global importance where to study past research.
deep-sea biota (Taviani 2002, 2014; Emig and Geistdoerfer
2004). Here, CWC occurrences taxonomically similar to
modern counterparts are best known from Neogene to 2.2 Cold-Water Coral Paleoecology
Quaternary sediments located along the Apennine chain in
peninsular Italy and Sicily, and on some islands in the Eastern According to the definition of Brenchley and Harper (1998)
Mediterranean (Di Geronimo 1987; Hanken et al. 1996; ‘Paleoecology attempts to discover and elucidate the life
Taviani et al. 2005a, b; Titschack et al. 2005, this volume; habits and relationships of fossil organisms to each other and
Roberts et al. 2009; Vertino et al. 2014, this volume; their surrounding environments’. This goal can be partly
Moissette et al. 2017). By large, those outcrops are of Early achieved by classical paleoecological reconstructions that
Pleistocene age, mostly ascribed to the Sicilian Stage. Late are aptly based upon the organisms’ ecological requirements
Pleistocene submarine CWC occurrences are instead distrib- (Ager 1963). In practice, paleoecology is continuously
uted basin-wide (Zibrowius 1980; Delibrias and Taviani evolving by gaining advantage of emerging disciplines,
1985; Taviani et al. 2005a, b, 2011a; McCulloch et al. 2010; improving technologies and methodologies, and by con-
Fink et al. 2015). stantly introducing new questions (e.g., Birks 1985, 2008;
The so-called ‘white corals’ Lophelia pertusa and Hunter 1998; Allmon and Bottjer 2001; Seddon et al. 2014;
Madrepora oculata sensu (Pérès and Picard 1964) are still Smiley and Terry 2017).
forming at present considerable bioconstructions and accu- As discussed in the present review, the literature consider-
mulations in the Mediterranean basin (Freiwald et al. 2009; ing CWC paleoecology is comparatively scant, reflecting the
Corselli 2010; Taviani et al. 2016; Wienberg and Titschack paucity of outcropping evidence and the relative inaccessi-
2017), thus making this region a significant CWC-carbonate bility of the submerged occurrences. Yet, the published stud-
factory (Titschack et al. 2016). ies contemplate both classical and frontier approaches.
2 Paleoecology of Mediterranean Cold-Water Corals 17
Fig. 2.1 Map of the Mediterranean region showing major sites men- ago; (6) Sardinia Channel; (7) Strait of Sicily; (8) Malta Escarpment;
tioned in the text: yellow circles correspond to outcrop occurrence, (9) northern Ionian Sea; (10) Santa Maria di Leuca; (11) Southern
white circles to submarine occurrences: (1) Sicily-Calabria; (2) Rhodes- Adriatic; (12) Crete; (13) Hellenic Trough
Karpathos; (3) Alboran Sea; (4) Balearic Islands; (5) Tuscan archipel-
The CWC habitats are inhabited by a variety of organisms biological activity (traces, borings, scars etc.) suitable to be
of highly different fossilisation potential. Organisms fossilised.
equipped with mineral parts typically have higher chances to
be preserved in the fossil record than soft body ones. The
geological survival of fossils depends upon a number of cir- 2.2.2 Diagenesis
cumstances, and also durable mineral parts are exposed
through time to profound alterations up to their total dissolu- The main engineers of CWC habitats are frame-building
tion, biasing the reconstruction of former communities and scleractinian corals which are aragonitic and thus prone to
from there extrapolating past environments. The complex easier post-mortem dissolution than, for example, co-
multi-facet filtering action of taphonomic and diagenetic occurring calcitic skeletons. The drilling of the giant
processes at the expense of a CWC community starts imme- Pleistocene Challenger Mound in the north Atlantic (IODP
diately post-mortem. 307) has provided a first-hand opportunity to evaluate CWC
aragonite loss before late burial alteration and lithification
take place. Frank et al. (2011b) hypothesise that the observed
2.2.1 Early Taphonomy selective aragonite dissolution (grain corrosion and fragmen-
tation) is caused by the corrosive action of undersaturated
Freiwald and Wilson (1998) have documented how complex pore waters, formed in response to organic matter oxidation.
and multistage are the early taphonomic processes affecting This process reverberates on the final preservation of arago-
a CWC habitat. As testified by their study of the Sula Ridge nite allochems (such as CWC) and delay at the same time the
CWC complex off Norway, early taphonomic processes lithification. It could thus bias the final fossil record and
encompass the formation of a biofilm and fungi over dead potentially the paleoecological assumptions. Although, inde-
Lophelia skeleton, propitious to the precipitation of the pendently by taxon, all CWC scleractinians are aragonitic, it
oxide patina and then the biofouling by a variety of inverte- is likely that their relative preservation potential in face of
brates as serpulids, brachiopods, foraminifers and bryozo- diagenetic processes varies according to their specific skele-
ans. Later taphonomic stages are documented by an increase tal microstructure and microarchitecture. This aspect, best
of sponges and bioerosion. One implication is that a CWC documented thus far for fossil shallow-water coral reef scler-
setting may experience many ecological turnovers on a rela- actinians (e.g., Dullo 1987), may be equally valid for CWC
tively short time-span (centuries to millennia), at times leav- and thus needs to be explored since it bears on the ultimate
ing a legacy beyond in the form of body fossils and/or correct paleoecological reconstruction.
cristagalli), Caryophyllia spp., Javania eburnea (= J. cail-

2.3 ode of Fossil Cold-Water Coral
M leti), Stenocyathus vermiformis, Enallopsammia scillae etc.
Occurrence The quantitative approach based upon the collection of a
standard volume of 1 dm3 of marly sediment is basically lim-
The reconstruction of CWC paleoenvironments needs to take ited to the study of the microfauna. With the exception of a
into account some specific contour aspects regarding their single volumetric sample of 3 dm3 from a sedimentary infill-
preservation mode. The approach differs noticeably if fossil ing, the whole of the macrofauna (which includes the CWC)
CWC are (i) hosted in loose sediment, (ii) plaster rocky sub- was instead handpicked as seen. The Valle Palione fossil
strates or (iii) are embedded in limestone. All such situations fauna is compared to living habits of extant organisms in the
are known to occur both in subaerial outcrop and under Atlantic and Mediterranean according to the bionomic
submerged conditions, and mixed situations are common- scheme proposed by Pérès and Picard (1964). Valuable envi-
place. Regarding outcrop evidence of the Mediterranean ronmental attributes of these Pleistocene communities (tro-
basin, these situations are best met in the Pleistocene CWC phic structure, salinity, temperature) have been thus derived
record of southern Italy, mostly in northeastern Sicily and through this actualistic approach. The Pleistocene succes-
Calabria (Barrier et al. 1989; Vertino 2003; Vertino et al. sion of Punta Mazza, Capo Milazzo (Sicily) hosts a corallo-
2013, this volume; Taviani, this volume, with references fauna which comprehends small, though frequent, fragments
therein), and on the Greek islands of Rhodes and Karpathos of the colonial M. oculata and E. scillae, presumably origi-
(Titschack et al. 2005; Moissette et al. 2017). Besides these nally attached to pebbles of the underlying conglomerate
two areas, records of fossil extant CWC are quite sporadic layer described by Fois (1990). The marly sediment is domi-
(Montanaro 1931; Placella 1980; Spadini 2015). nated by soft-bottom solitary corals, such as Balanophyllia
In the case of CWC associated with unlithified sediment, cellulosa inhabiting at present circalittoral to epibathyal
individual components, that are often reasonably well pre- environments of the Mediterranean. The Punta Mazza coral-
served within a clay matrix, could be extracted for taxonomic bearing deposit has been interpreted by Vertino (2003) as to
identification and are also available to refined taphonomic represent an epibathyal setting.
assessment (mineralogy, bioerosion, etc.). In principle, this Colella and D’Alessandro (1988) propose that the pres-
CWC preservation is ideal for quantitative analyses based ence of L. pertusa and M. aff. oculata branches and other
upon standard volumetric sampling. megafauna in the Pleistocene megabreccia topping the
We discuss below only the modern literature that Monte Torre succession (Calabria) is due to sediment gravity
approaches, at a various degree of deepening, paleoecologi- flows, likely in a paleostrait context. These authors report
cal aspects of CWC-bearing deposits. No reference is made also a third species of extant colonial CWC, Solenosmilia
at the historical bibliography on fossil extant-type CWC, variabilis, but this proved to be a misidentification of a mis-
which can be found in Taviani et al. (2005a, b) and Vertino shapen Lophelia (Zibrowius 1991).
et al. (2014). Pleistocene CWC-bearing deposits also occur on the
island of Rhodes (Titschack and Freiwald 2005). Here, L.
pertusa branches embedded in marly sediment at the Lardos
2.3.1 Outcrop SW Hill site are interpreted by Titschack et al. (2013) as rep-
resenting a displacement of these corals due to a debris flow
2.3.1.1 Cold-Water Corals Hosted in Loose in a ‘blind’ paleocanyon setting. Bromley (2005) produced a
Sediment comprehensive evaluation of the bioerosion of Lophelia
Placella (1979) comments upon the CWC fauna from Archi branches in the Pleistocene Lindos Bay clay. Some 18 differ-
(Reggio Calabria) containing Lophelia pertusa among other ent ichnotaxa have been identified, referred to the activity of
deep-sea scleractinians. The author estimates a paleodepth boring fungi, polychaetes, sponges and phoronids, attach-
between 1000–1500 m based on the modern distribution of ment scars attributable to foraminifera, brachiopods and
scleractinian corals and temperature up to 11 °C using bivalves and gnawing marks due to echinoids.
Madrepora as an actualistic example. Ruggieri et al. (1979)
report the occurrence of a fauna that includes L. pertusa and 2.3.1.2 Cold-Water Corals Plastering Hard
Madrepora oculata in the Pleistocene of Primosole (Siracusa, Substrates
Sicily) as one of the supporting evidence pointing at bathyal Published examples of fossilised CWC plastering hard sub-
conditions at the time. Di Geronimo (1979) describes a strates (such as hardgrounds) are only a few and those are
highly diverse Pleistocene bathyal fauna at Valle Palione often associated or interspersed with mobile bottoms.
(Catania, Sicily) containing, among other invertebrates, the Barrier et al. (1996) describe one such occurrence in the
‘white corals’ L. pertusa, Madrepora aff. oculata, and many Pleistocene of Lazzàro (Calabria) where individual boulders
other scleractinians such as Desmophyllum dianthus (as D. lay onto clay sediments at the base of a paleoescarpment.
Boulders are fouled by the deep-water scleractinians L. per- Vertino 2003; Stolarski and Vertino 2007). Several
tusa, M. aff. oculata, E. scillae, D. cristagalli (= D. dian- Pleistocene CWC outcrops of northeastern Sicily are consid-
thus), Caryophyllia sarsiae and other co-occurring organisms ered by Vertino (2003) and Vertino et al. (2013) that provide
(bivalves, barnacles, octocorals etc.). The paleoecological paleoecological information. Some of the coral-dominated
reconstruction based upon field evidence and the fossil limestones in the surroundings of Messina, are interpreted as
assemblages of both clay sediment and boulders, envisages a bioconstructions in place or as extensive coral rubble aprons
bathyal setting at the foot of a submarine escarpment where (Vertino work in progress). In particular, the succession at
coral growth was suddenly stopped by rapid silting. A simi- ‘La Montagna’ contains extant CWC whose preservation
lar situation has been observed at Vallone Catrica, Calabria ranges from almost pristine, and embedded in a semilithified
(Di Geronimo 1987) and in Sicily at Capo Milazzo, San matrix, to partly or completely dissolved up to leave only
Filippo and Camaro where isolated boulders, presumably vugs or molds (Vertino 2003; Vertino et al. 2013). In the view
fallen from paleocliffs, were exploited by CWC and, in some of Barrier et al. (1985), the succession was a large submarine
cases, deep-water giant oysters (Vertino 2003; work in prog- dune to account for bed thickness and presence of mega
ress). The case-study analysed by Di Geronimo et al. (2005) cross-bedded basal deposits. Titschack et al. (2008) and
at Furnari (NW Sicily) is rather interesting and somewhat Vertino et al. (2013) consider the option that La Montagna is,
unique, combining the encrustation of a lithified steep sub- at least partly, a former CWC mound since coral fragments
strate (possibly a former hardground) along a fault plane are often large and their abrasion low, suggesting a parau-
with the loose infilling within fissures by clayey sediment tochtonous source instead than intense bottom-current
rich in CWC rubble and a quite diverse associated benthic reworking solely. These authors envisage a depositional
fauna. The proposed paleoecological reconstruction calls for model that combines an initial submarine-dune phase, then
a situation where the steep substrate was originally settled by followed by in situ accretion with corals baffling sediment
CWC, whose basal parts can be still found attached to it and and further creating lithified substrate to following growth
detached remains are now found in the adjacent clayey sedi- through early diagenetic processes.
ment and fissures. Information that could turn useful in evaluating paleoeco-
Early Pleistocene hardgrounds and carbonate surfaces logical aspects may be derived also by partially or totally
encrusted by extant CWC have been identified by Moissette dissolved CWC in limestones, through opportune ‘recovery’
et al. (2017) on the Sokastro islet and at Levkos, Karpathos techniques such as molding or microtomographic imaging.
islands, Greece. The corallofauna comprehends species If CWC-bearing limestones are highly lithified, taxo-
requiring hard substrate to settle as well as others living in nomic and paleoecological information (including presence
the sediment. These authors list a number of colonial and of symbionts, boring traces, etc.) must be derived from the
solitary scleractinian CWC (L. pertusa, M. oculata, study of polished and thin sections. A case in point are the
Enallopsammia sp., Dendrophyllia cornigera, D. dianthus, Pleistocene limestones containing L. pertusa, M. oculata and
S. vermiformis, Flabellum alabastrum, Caryophyllia sarsiae, D. dianthus reported from Rhodes (St. Paul’s Bay limestone)
C. smithii), as well as isidid corals (Keratoisis sp.), that have been analysed by Titschack and Freiwald (2005).
Corallium sp., molluscs, barnacles, serpulids and bryozoans. By integrating field evidence, CWC ecological requirements
Based upon the benthic assemblage, containing not only and microborings, Titschack and Freiwald (2005) recon-
‘white corals’ but also characteristic cirripeds (Pachylasma structed a cliffed rocky environment for the St. Paul’s Bay
giganteum) and bivalves as the giant deep-sea oyster limestone, characterised by the presence of hardgrounds,
Neopycnodonte zibrowii (see Wisshak et al. 2009) and the debris flows and Neptunian dykes in a depth range of 300–
large limid Acesta excavata (see López Correa et al. 2005), 500 m. Interestingly, Titschack and Freiwald (2005) present
these authors reconstruct an upper bathyal paleoenvironment in their study an ecological detail of these ancient CWC hab-
at an estimated paleodepth of 400–600 m with bottom tem- itat clearly pointing out at the presence of the commensal
peratures cooler than today. polychaete Eunice (Roberts 2005), based upon a thin section
of its calcified tube.
2.3.1.3 Cold-Water Corals Embedded Other examples of CWC-Pleistocene limestones, hosting
in Limestones D. dianthus, as well as the deep oyster N. zibrowii, occur at
Limestones embedding CWC may show advanced diage- Punta Gamba di Donna, Punta Milazzo, Sicily (Rosso et al.
netic processes that could obviously mask primary morpho- 2013), but their paleoecology has not been studied in any
logical features preventing coral identification. This holds detail to date. A Pleistocene Desmophyllum-limestone inter-
true for aragonitic scleractinians prone to partial to total dis- preted as a representing a paleocliff encrustation at bathyal
solution. In the latter case, coral identification is still possible depths is illustrated by Di Geronimo (1987: Pl 3 fig 4) from
if the fine grain-size of the embedding sediment allows the the Pleistocene of Vallone Catrica, Calabria. Part of the
preservation of the coral outer wall micromorphology (cf. paleobiological CWC record from the Sokastro islet site
also belongs to this category (Moissette et al. 2017, figures oxide patination are commonly observed in the Mediterranean
3 and 4). Sea (Bernoulli and Mc Kenzie 1981; Biju-Duval et al. 1983;
In summary, the main paleoecological outcome of many Allouc 1990; Remia et al. 2004; Toscano and Raspini 2005;
published contributions related to outcrop evidence is the Conti et al. 2013). Cold-water corals are found embedded
reconstruction of the former bathymetry and paleocommu- into hardgrounds (Taviani and Colantoni 1984; Zibrowius
nity taxonomic composition. Because of the relatively wide and Taviani 2005; Vertino et al. 2010; Angeletti and Taviani
vertical distribution of L. pertusa, M. oculata and D. dianthus 2011; Taviani et al. 2011a), and this may result conservative
in the Mediterranean and elsewhere in the ocean, any paleo- of the corals (Fig. 2.2), including their original mineralogy
bathymetric interpretation cannot provide a strict figure but by subtracting them at the action of aggressive waters. The
only a range. Noticeably, already Seguenza (1864) correctly hardground itself is an ideal surface for CWC settling
understood that the fossil coral fauna from the surrounding of (Fig. 2.3), together with other encrusting fauna (Taviani et al.
Messina (southern Italy) was of considerable depth, notwith- 2005b, 2010, 2011a, b, 2016; Freiwald et al. 2009; Rosso
standing the scarce knowledge on deep-sea ecosystems at that et al. 2010; Angeletti et al. 2014; Sartoretto and Zibrowius
time (Taviani, this volume; Vertino et al., this volume). 2017). Ecological turnovers are to be expected on a surface
In this respect, the reconstruction offered by Di Stefano exposed for a while in the water column, as often docu-
and Longhitano (2009) of a Pleistocene paleo-strait deposit mented by encrusters at different degree of preservation and
containing CWC fossil fauna in the Peloritani chain in the patination (Fig. 2.2). The temporal discrimination among the
Messina area (La Montagna, San Filippo and other classic settlers of even a single surface would not be possible if not
successions) as formed in a tidal setting is rather difficult to assisted by multiple dating of individual skeletons.
understand. These authors hypothesise, in fact, that deposits Overall, the main difference from outcrop deposits is that
containing only deep-water species, including L. pertusa, M. by large these coral communities and associated organisms
oculata, E. scillae, D. cristagalli (= D. dianthus) and typical have never been exposed to taphonomic processes under
bathyal species from other taxonomic groups, formed in a subaerial conditions, above all leaching by meteoric waters
shallow-water context under enhanced water turbidity, disre- or precipitation of non-marine cements. Thus, with respect to
garding the ecological incongruence embodied by CWC. outcrop situations (see Sect. 2.3.1), the mode of occurrence
At any event, the presence of these deep-water corals and of Late Pleistocene submarine Mediterranean record includes
associated fauna has been sufficient to provide a robust sup- CWC either “Cold-water corals hosted in loose sediment” or
port to geodynamic reconstructions, such as the strong uplift “Cold-water corals plastering hard substrates” while the case
of the (paleo) Messina Strait margins in eastern Sicily and of “Cold-water corals embedded in limestones” should be
southwestern Calabria (e.g., Barrier et al. 1986, 1990, 1992; considered rather uncommon. This submarine record is quite
Montenat et al. 1987). important for a better assessment of on-land situations
because, apart for the poorly-fossilisable components, its
fossil legacy is intrinsically close to the original ecological
2.3.2 Submarine Occurrences situation since less affected by later, often destructive diage-
netic processes. Furthermore, it permits in many cases to
Pre-modern CWC are widespread in the Mediterranean basin precisely date individual components to disclose with confi-
(Delibrias and Taviani 1985; Taviani et al. 2005a, b; dence subtle ecological turn-over through time, what is at
McCulloch et al. 2010; Margreth et al. 2011; Fink et al. present almost impossible for the time-averaged and undat-
2015), and are often degraded and patinated if exposed to the able Early-Middle Pleistocene and older situations.
seafloor (Blanc et al. 1959; Hersey 1965; Selli 1970; In the past, subfossil CWC have been routinely obtained
Bellaiche et al. 1974; Zibrowius 1981; Remia and Taviani through heavy geological dredges operating on structural
2005; Gamberi et al. 2006; Rosso et al. 2010; Angeletti and highs such as seamounts or escarpments (Selli 1970;
Taviani 2011; Sartoretto and Zibrowius 2017). Extensive U/ Bellaiche et al. 1974; Cita et al. 1979; Taviani and Colantoni
Th-dating has documented that they are mostly of middle to 1984; Allouc 1987; Taviani et al. 2005a, b, 2011b; Zibrowius
late Pleistocene covering ages from ca 480 kyrs up to the and Taviani 2005; Gamberi et al. 2006, with references
Holocene, although most dates are post-Last Glacial therein). For long the modest optical resolution offered by
Maximum (McCulloch et al. 2010; Fink et al. 2015). research submersibles did not permit any refined paleoeco-
Deep-water settings, especially on sloping topography logical appreciation from in situ images (see, for examples,
and under the influence of bottom currents, can be the site of the images in Allouc 1987). Thus, paleoecological informa-
a complex process of submarine lithification of the muddy tion was derived for a while by the qualitative inspection of
sediment ultimately ending into a hardground (Noé et al. dredged samples examined in the laboratory. An exception is
2006; Rebesco and Taviani, this volume). As for the open the study by Zibrowius (1981) based upon the Cyana manned
ocean, more or less advanced micritisation and subsequent submersible and reporting over the subfossilised benthos
Fig. 2.2 Examples of

preservation of fossil CWC
from submerged situations in
the Mediterranean Sea: (a)
polished section of a micritic
limestone embedding the
solitary scleractinian
Desmophyllum dianthus;
external surface patinated by
Fe-Mn oxides: Malta
Escarpment, ca. 2000 m
depth, bar = 5 cm; (b)
CWC-bearing framestone
with large D. dianthus coral
welded to the surface, observe
patination and later
encrustation by serpulid
polychaetes; northern Ionian
Sea (39°03′ N – 18°54′E),
1200 m depth, bar = 5 cm.
(Photographs: a, b: © ISMAR-
CNR Bologna)
Fig. 2.3 Examples of CWC situations versus coring: (a) A loose CWC- but a paleoecology analysis could be performed through Dohrn Canyon,
canopy partly buried in mud could be targeted for gravity or box-coring; Gulf of Naples, −390 m; bar = 2 cm. (Photographs: a, b: © ISMAR-
Nora Canyon, Sardinia Channel, −420 m, bar = 20 cm, (b) precipitous CNR Bologna)
topographies exposing CWC on hard bedrock are unsuitable to coring,
(scleractinians, serpulids), inclusive of Atlantic-type CWC, and of their present distribution in the north Atlantic Ocean,
encrusting patinated hardgrounds from the Hellenic Trough. the authors speculate that those taxa participated to former
Taviani and Colantoni (1979) analysed the co-occurrence of ‘white coral’ communities that inhabited the glacial
subfossil Lophelia, Madrepora and Desmophyllum together Pleistocene Mediterranean at temperatures not exceeding
with the large bivalve Lima excavata (= A. excavata) and the 10.4 °C. Taviani and Colantoni (1984) described a Last
corallivorous gastropods Coralliophila lactuca (= C. rich- Glacial fossil assemblage recovered by dredging the Malta-
ardi) and C. lamellosa (= Hirtomurex squamosus) in tapho- Siracusa escarpment at depths below 2000 m, and character-
coenoses dredged in the Strait of Sicily and Balearic Sea ised by the co-occurrence of the CWC D. cristagalli (= D.
between 300 and 700 m. In absence of any dating and on the dianthus) and the pectinid Delectopecten vitreus. Fossils are
basis of the ecological consistency represented by the fre- embedded within a Fe-Mn-oxide patinated micritic lime-
quent and intimate association of such CWC and molluscs at stone which plasters cliffs of the escarpment. Originally
present (see López Correa et al. 2005; Taviani et al. 2009), interpreted by the authors as representing a single fossilised
biocoenosis, it is instead likely that the bathyal pectinids depth, of subfossil Holocene CWC frames (Madrepora and
settled over and inside dead Desmophyllum calices, therefore Lophelia) entrapping shells of corallivorous gastropods
at later stage of colonisation of the substrate. In fact, D. vit- (Muricidae-Coralliophilinae, Architectonicidae). The coral
reus is often but not exclusively associated with fossil frame acted as a taphonomic trap to rare cnidarian-predatory
(Barrier et al. 1996; Sartoretto and Zibrowius 2017) and organisms ecologically coherent with a CWC habitat. The
recent CWC habitats (Mastrototaro et al. 2010; Panetta et al. final preservation of both corals and molluscs was then
2010; Taviani et al. 2011a). enhanced by early submarine lithification and patination.
Manned submersible surveys in the Stoechades Canyon
off the Provence coast of France recently documented that
cliffs and large boulders between 1700–220 m appear 2.3.3 CWC in Sediment Cores
intensely fouled by subfossil black-patinated D. dianthus, C.
sarsiae and J. cailleti, plus a number of associated inverte- As seen before, most previous work on submerged CWC
brates such as serpulids (Neovermilia falcigera and sites dealt with hand-samples, often recovered through
Filogranula stellata), molluscs and octocorals (Sartoretto poorly positioned geological dredging, and at a considerably
and Zibrowius 2017). The age of this thanatocoenosis is lesser degree, observation by manned submersibles. The
unknown but, in all likeness, (late?) Pleistocene in analogy technological and scientific advancement in the exploration
with comparable situations in the Mediterranean Sea as the of the deep brought a breaking novelty in the field of CWC
Malta-Siracusa escarpment case-study mentioned above. paleoecology, which is coring.
The case-studies recorded by Taviani and Colantoni (1984), Cold-water coral grounds are intrinsically difficult to core
Zibrowius (1991), Taviani et al. (2011a); Sartoretto and for the following reasons: (i) They are often located at rocky
Zibrowius (2017) corals plastering hard substrates” and, sites where the predominant substrate discourages any cor-
partly, incipient stages of “Cold-water corals embedded in ing attempt, (ii) they may be located on precipitous almost
limestones” categories discussed in the 2.3.1 section. vertical topographies unsuitable to coring, (iii) they may be
Late Pleistocene Madrepora-dominated reefs occur partly lithified posing a problem to traditional (piston, grav-
between 355–410 m offshore the Tuscan archipelago in the ity) coring, (iv) they may be very reduced in size and difficult
Tyrrhenian Sea. Remia and Taviani (2005) describe coral to locate without visual inspection, making useless random
carbonates, part of which oxide-patinated, providing some coring, (v) their texture could be very intricate making a
paleoecological hints. The framestones embed shells of ben- coral canopy unsuitable to easy coring (Fig. 2.3).
thic invertebrates like molluscs (coralliophiline and limpet These caveats and the little interest around CWC until
gastropods) and brachiopods (Megerlia truncata, Gryphus 20 years ago explain the virtual lack of coring documenta-
vitreus) consistent with CWC habitats (cf. Taviani et al. tion for long. Among the few exceptions is the pioneer work
2017). The subfossil CWC frames display also the presence by Ayers and Pilkey (1981) on CWC grounds off the US
of Eunice encalcified tubes denouncing the former presence eastern Atlantic margin. Improved mapping techniques (such
of this commensal polychaete in the Pleistocene reefs, and as multibeam), direct bottom inspection through TV-equipped
ichnologically diagnostic scars and pitting documenting the devices (for example, large box-corer), the assistance pro-
activity of brachiopods (Novocrania anomala) and attached vided by ROV in selecting best potential sites, the availabil-
foraminifera, respectively. This case-study (as most of CWC ity of aptly drilling vessels and new coring techniques (for
core-evidence, see below) attains at the “(i) Cold-water corals example MeBo: Freudenthal and Wefer 2007) have disclosed
hosted in loose sediment “category discussed in the ‘Outcrop’ new horizons in the study of CWC by achieving geo-
section. referenced successions with their original stratigraphy. Thus,
Based upon remotely operated vehicle (ROV) images and since the mid ‘90s the scenario has changed considerably
bottom samples, Rosso et al. (2010) recognised six ‘thanato- and coring (piston, gravity and box) is routine on most
facies’ at the Santa Maria di Leuca CWC province in the research conducted on Atlantic (Dorschel et al. 2005;
Ionian Sea, established on skeletonised components shed by Rüggeberg et al. 2007; Hebbeln et al. 2008, 2009; Wienberg
calcifying organisms. Although not per se a real paleoeco- et al. 2009, 2010a, b, 2018; Frank et al. 2011a; Freiwald
logical study s.s., this exercise has the value to provide snap- et al. 2011; Van Rooij et al. 2011; Douarin et al. 2013;
shots on post-mortem CWC-related assemblages formed in a Vandorpe et al. 2017) and Mediterranean CWC (Malinverno
relatively short time span. As introduced before, this kind of et al. 2010; Freiwald et al. 2011; Margreth et al. 2011; Fink
information may assist interpretation of time-averaged situa- et al. 2012, 2013, 2015; Douarin et al. 2014; Titschack et al.
tions seen in outcrop, difficult to unravel since evidence 2016; Dubois-Dauphin et al. 2017).
beyond radiometric dating techniques. To this, it must be added the successful drillcoring off
Angeletti and Taviani (2011) reported the peculiar case, Ireland of the Challenger Mound (Belgica Mound Province,
from the South Malta CWC province at ca. 680 m water Porcupine Seabight) during Expedition 307 of the Integrated
Ocean Drilling Program (IODP). A total of three holes CWC (reviewed by Montagna et al. 2011; Robinson et al.
(U1316, U1317, U1318) recovered a long record reaching 2014; Montagna and Taviani, this volume). This could be,
down to the upper Pliocene (Ferdelman et al. 2006b; Kano for instance, an important aid and independent approach at
et al. 2007; Thierens et al. 2009). determining more precisely variables as seawater tempera-
Coring makes available to the scientific community an ture, at constraining salinity and nutrient concentration, and
unprecedented archive of CWC-bearing situations prone to be understanding response to ocean acidification, but is seldom
studied under various paleoecological perspectives. To date, introduced in a standard paleoecological study. Within the
most attention on the core record concerns, in fact, the onset/ scheme of a modernised approach to paleoecology (Seddon
demise of CWC through time, and the identification of possi- et al. 2014), it is easy to foresee that CWC geochemistry will
ble forcing ecological, climatic and oceanographic factors. get more and more momentum.
Paleoecology here merges, therefore, into paleoceanography
with most arguments focusing on the presence or absence of
emblematic CWC and their precise chronology. Less has been 2.5 Discussion
produced about the response to environmental factors of the
biological component in a core record, and holistic studies As seen, not much has been written thus far on the paleoecol-
encompassing the whole fossil content have yet to be ogy of Mediterranean CWC with respect of its enormous
produced. potential. Fragmented or specific information on some basic
Regarding the Mediterranean, Margreth et al. (2011) taphonomic or paleoenvironmental aspects predominates with
reconstruct contour conditions around CWC growth in the respect to a more comprehensive paleoecological analysis. In
mud volcano area of the west Alborán Sea using the core’s principle, the paleoecological analysis of CWC in outcrop
planktonic and benthic foraminifer record. Finally, Stalder appears intrinsically easier than producing similar studies in
et al. (2015) produced one of the most comprehensive and the deep sea. However, the evidence gained from the study of
quantitative study of CWC-bearing cores. By examining still-submerged late Pleistocene-Holocene occurrences warns
quantitatively the abundance of macrofossils (scleractinians, about potential problems in interpreting a fossil situation. U/
bryozoans and others) and microfossils (foraminifers and Th-dating of CWC recovered from a very steep wall from the
ostracods) in cores from the Alborán Sea, the authors recon- Balearic escarpment at >900 m may help to elucidate
struct various environmental factors such as flux and type of this issue. The sample consisted of two specimens of
nutrients, bottom currents, seawater temperature and density, Desmophyllum dianthus one attached on each other, the exter-
oxygenation, sediment supply that exert control on CWC nal one being alive whilst the second was dead (Fig. 2.4). Up
growth, turnover or demise through time. All such cases per- to 10,000 years separate the two corals sitting on each other
tain by large to the “(i) Cold-water corals hosted in loose that settle precisely the same spot (Montagna et al. 2006).
sediment” category discussed previously. Only the precise radiometric chronology exposes an otherwise
hidden pulsing colonisation of the area, characterised by times
of CWC recession. Such type of subtle, albeit relevant eco-
2.4 Paleoenvironmental Information logical turnovers cannot be disclosed in outcrop situations
Derivable from Geochemical Signals which are beyond the potential of dating techniques.
A modern paleoecological approach to the study of
The main constraint in interpreting the geochemical signals hardground and other rocky substrates encrusted by CWC
of the aragonite skeleton of fossil coral remains from sub- should consider importing methodologies, with opportune
aerial outcrop is the presence of diagenetic alterations. adaptations, typically applied to live communities, in partic-
Dissolution and recrystallisation of the skeleton can disrupt ular habitat mapping by means of ROV (Vertino et al. 2010;
the primary geochemical signal, strongly limiting the inter- Savini et al. 2014; Bargain et al. 2017, 2018; Angeletti et al.,
pretation of the geochemical proxies. Screening for traces of this volume-a, this volume-b; Lo Iacono et al., this volume).
diagenesis, such as micro-dissolution, secondary cements or This would represent a major goal when applied to the most
aragonite to calcite recrystallisation, is thus a necessary step topographically difficult situations, such as steep canyons or
when investigating the geochemistry of fossil corals long walls. The Mediterranean basin provides a number of such
exposed to subaerial conditions (e.g., Janiszewska et al. sites with known subfossil CWC occurrences, as for example
2017). Micro-analytical techniques like laser ablation the Balearic Islands margin, the Malta Escarpment, the Crete
ICP-MS or ion microprobe can partially overcome this limi- margin, the Bari Canyon in the Adriatic, and many sea-
tation through a selective sampling strategy that targets pris- mounts in the Tyrrhenian and Ionian seas.
tine skeletal portions (Montagna and Taviani, this volume). There is an enormous potential for conducting detailed
Valuable environmental information could be extracted paleoecological analysis on past CWC habitats by using the
through the geochemical composition of fossils, such as superb, but largely underworked, record provided by cores.
Fig. 2.4 Hand samples

showing complex patterns of
re-colonisation; (a) Living
Desmophyllum growing on a
framestone encrusted by
Pleistocene corals; observe
differential patination; from a
steep wall at 800 m water
depth, Balearic Islands;
bar = 1 cm; (b) multiple
generations of solitary corals
and serpulids encrusting a
fossil internal valve of the
giant oyster Neopycnodonte
zibrowii, Balearic Islands, >
800 m; bar = 1 cm.
(Photographs: a, b: ©
ISMAR-CNR Bologna)
Fig. 2.5 Examples of CWC

contained in cores: (a) Coral
fragments hosted in muddy
sediment within a split gravity
core (Adriatic Sea),
bar = 5 cm; (b) computed
tomography discloses
presence and fabric of CWC
inside a core; resolution
permits taxonomic assessment
at species level (Madrepora
oculata); Strait of Sicily,
Linosa island, −600 m,
bar = 5 cm. (Photographs: a,
b: © ISMAR-CNR Bologna)
Standard qualitative and quantitative approaches can be now species-level), relevant for the paleoecological reconstruc-
take advantage of computed tomography at the scale of the tion (Fig. 2.5).
core (López-Correa et al. 2007; Tanaka and Nakano 2011; Microtomography instead permits to resolve with great
Douarin et al. 2014; Victorero et al. 2016; Wienberg and detail hidden internal features, microarchitecture and bioero-
Titschack 2017; Angeletti et al., this volume-b) and of sion paths (e.g., Beuck et al. 2007; Zapalski and Dohnalik
microtomography (Beuck et al. 2007; Färber et al. 2016) at 2013; Lee et al. 2017). Ultimately, its interactive application
the scale of individual fossils. Computed-tomography will allow to study CWC through the creation of 3D digital
images are excellent in providing the 3D spatial arrangement modeling, the field of virtual paleontology (Sutton et al.
of CWC and any other associated fossil (up to taxonomy at 2014).
2.6 Conclusions and Future Research correct interpretation of the corresponding fossil ones.
Sampling would be a major challenge when dealing with
We have presented and discussed the progress of science and encrusters on a hardground or on a wall but recovering fos-
the current perspectives for tackling with CWC paleoecology. sils is a relevant part of a CWC paleoecological assessment.
Pre-modern, by large Pleistocene, scleractinian CWC occur- Specifically designed and properly mounted microdrills may
rences are common place as submarine situations in the whole be considered for this action whenever a manipulator arm
Mediterranean Sea and, far less as outcrops at specific sites of would fail.
this basin. Their preservation mode varies considerably what In all likeness, drilling will be implemented more and
deeply influences the quality of ecological restitution. more to sample long sedimentary succession containing
The refined paleocological interpretation of CWC occur- CWC, bearing upon improvements in the design of the
rences and their functioning through time will greatly benefit related equipment as well as on their support vessels.
by the on-going advancement of knowledge on biological
traits of participating organisms (taxonomy, ecology, physi- Acknowledgements This chapter is dedicated to Jean Pierre Henriet
ology) in the modern deep-sea habitats. The contribution (1945–2017), a friend and a colleague, to honor his prominent contribu-
tion to unveil the geological importance of cold-water corals. We are
offered by the other scientific fields, like geochemistry, is indebted to Helmut Zibrowius and three anonymous referees for their
further widening the prospects in paleoecology. Certainly, positive and useful comments to improve the clarity of the text, and to
the application of integrated paleoecological approaches Covadonga Orejas and Carlos Jiménez for editorial work. The current
would affect positively the reliable analysis of the on-land understanding of extant deep-water coral taxonomy, biogeography and
spatio-temporal distribution owns immensely to the research activity of
and submerged situations like those recorded in this Helmut Zibrowius at sea and on-land. His keen and meticulous under-
chapter. standing of North Atlantic and Mediterranean coral taxonomy has been
The implementation of virtual paleontology in the study the source of inspiration for all subsequent studies in the field. This
of CWC will prove instrumental in the understanding at fine paper is Ismar-Bologna scientific contribution n. 1933, and is part of
EU F.P. VII Projects COCONET, (contract no. 287844), and EVER-
resolution of internal coral structures and diagenetic pro- EST (contract no. 674907), DG Environment programme IDEM (grant
cesses, useful to better decipher important paleoecological agreement No 11.0661 /2017/750680/SUB/EN V.C2), and the Flag
traits. Project Ritmare (Ricerca Italiana per il Mare) project.
New frontiers are obvious in the deep sea. In the specific
case of conducting paleoecological research on submerged
CWC sites, research gets and will get benefit of the phenom- References
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Drop Chapter
Cold-Water Corals in the Mediterranean: 3
A History of Discovery
Julian Evans, Leyla Knittweis, Joseph A. Borg,

and Patrick J. Schembri
Abstract The existence of cold-water corals (CWC), such as the

The earliest records of cold-water corals from the framework-building Madrepora oculata Linnaeus 1758 and
Mediterranean Sea date back to the eighteenth century Lophelia pertusa (Linnaeus 1758) and associated solitary
when Linnaeus first described Madrepora oculata based coral Desmophyllum dianthus (Esper 1794), has been known
on specimens from the central Mediterranean and for at least half a millennium, as attested by the lists of syn-
Tyrrhenian Sea. It was only towards the end of the nine- onymies dating back to the sixteenth century given by Milne
teenth century that cold-water corals were recorded from Edwards and Haime (1850). The first Mediterranean record
elsewhere in the Mediterranean, thanks to early research is possibly that by Marsilli (1725), whose figure of M. ocu-
cruises that explored the Mediterranean deep-sea benthos. lata could have been based on specimens collected off
Although the first records of live cold-water corals date Marseille (Zibrowius 1980). However, the first confirmed
back to the early twentieth century, further observations record seems to be by Linnaeus (1758), who named and
of living individuals were extremely rare and most records described M. oculata on the basis of specimens collected
made by the end of the century were actually based on from the “Mari Siculo, Tyrrheno” (central Mediterranean
dead or fossil fragments. This led to the idea that extant and Tyrrhenian Sea). Linnaeus’ type specimens are missing,
Mediterranean cold-water coral assemblages are merely so it is not clear if his description was based on live, dead, or
relicts of the communities that thrived during the even fossil fragments. Fossils of several taxa contributing to
Pleistocene. However, several sites with live framework- present-day CWC assemblages date back as far as the
forming cold-water coral species were discovered since Miocene epoch, with these fossil genera being morphologi-
the year 2000, including six regions identified as cold- cally indistinguishable from extant ones (Taviani et al. 2011).
water coral provinces given that they support a dense Specimens dredged from the deep sea may represent fossil
growth of living corals. The emerging picture is that thriv- forms dating back to the Pleistocene, and these are not
ing cold-water coral assemblages that are hotspots of always easy to tell apart from more recent specimens as they
deep-sea biodiversity still occur in the Mediterranean, but can lack the dark coating of iron-manganese oxides typical
have a rather punctuate distribution along the circulation of hard material in deep water (Zibrowius 2003). Historical
path of the Levantine Intermediate Water, which appears records of CWC based on dead material must therefore be
to be a main driver for cold-water coral distribution in the interpreted with caution, particularly since Mediterranean
Mediterranean. CWC assemblages appear to have had a much more exten-
sive distribution during the Pleistocene than at present.
Keywords Until recently, most records of CWC species from the
Benthic biodiversity · Coral framework · Historical Mediterranean were actually based on dead (or subfossil/fos-
records · Oceanographic expeditions · Scleractinia sil) fragments. The earliest such records are of M. oculata,
and these were most likely based on specimens brought up
unintentionally in commercial red coral fisheries by collect-
ing gear which had been lowered into deeper waters; the
branches present in various old museum collections gener-
ally lack any indication of origin but were probably sourced
J. Evans · L. Knittweis · J. A. Borg · P. J. Schembri (*) from the Tyrrhenian Sea and Sicilian waters (Zibrowius
Department of Biology, University of Malta, Msida, Malta 2003). More precise information is available starting from

https://doi.org/10.1007/978-3-319-91608-8_3
32 J. Evans et al.
the late nineteenth century, based on records made during to that associated with the extensive CWC frameworks of the
early research cruises that explored the Mediterranean deep- north-eastern Atlantic. Zibrowius (2003) cautioned that it is
sea benthos. The history of discovery of CWC in the unrealistic to compare the species richness of the intensely
Mediterranean closely follows that of the deep-sea explora- studied Atlantic CWC communities with that of their much
tion of this region, starting with the Porcupine (1870) expe- less well-studied Mediterranean counterparts, and that it is
dition, which recorded the presence of both M. oculata and unlikely that the Mediterranean “white coral” communities
L. pertusa in the Sicilian Channel (Duncan 1873; see also are in fact species poor (for an updated review see Rueda
Taviani, this volume). By the end of the twentieth century, et al., this volume). On the other hand, the dearth of records
further records were made during cruises by the Washington of live CWC made by the end of the twentieth century
(1881–1883), Princess-Alice and Hirondelle (1888–1922), supported the notion that extant Mediterranean CWC
Pola (1890–1893), Valdivia (1898–1899), Calypso (1954– assemblages are merely relicts of the communities that
1964), Jean Charcot (1972–1974), Hannoun (1973), Cryos thrived during the Pleistocene.
(1984), Suroit (1995), Europe (1996), Sonne (1996), and In 2000, several living colonies of M. oculata and L. per-
Urania (1996–2000) (see Zibrowius 1980, 2003). Most of tusa and individuals of D. dianthus were accidentally col-
these records were based on dredged specimens, but direct lected during experimental fishing operations off Cape Santa
observations were also made through manned submersibles Maria di Leuca, representing the only large live Lophelia-
such as the Cyana, Griffon, the French bathyscaphe, and bearing deep coral area known at the time (Mastrototaro et al.
Jacques Cousteau’s diving saucer (SP350 Denise) (Zibrowius 2002). Just 3 years later, a second area with living Madrepora–
2003). Lophelia–Desmophyllum CWC was discovered south of
The first confirmed records of live Mediterranean CWC Malta, again incidentally during experimental trawl surveys
date back to the early twentieth century: in 1910 L. pertusa (Schembri et al. 2007). These discoveries led to extensive
and D. dianthus were found alive on a telegraph cable in the studies in the areas, including through dedicated oceano-
vicinity of Cabo de Gata (Alborán Sea), and subsequently a graphic research cruises such as those by the R/V Meteor and
living specimen of M. oculata was collected from off north R/V Urania. In the meantime, several other sites with live
Sicily in 1922 (see Zibrowius 1980). By the end of the framework-forming CWC species were also discovered,
century, the only other records of live individuals of M. extending from the Strait of Gibraltar to Cyprus and including
oculata were those made in canyons near Banyuls (Lacaze- localities in the Alborán Sea, the Gulf of Lions (Cap de Creus,
Duthiers canyon) and Marseille (Cassidaigne canyon), and Lacaze-Duthiers, and Cassidaigne canyons), the Ligurian and
south of Thassos Island in the northern Aegean Sea. Besides Tyrrhenian Seas, the central Mediterranean, and the southern
the Cabo de Gata specimen, additional records of live L. Adriatic and northern Aegean Seas (Taviani et al. 2017;
pertusa were even rarer, restricted to off Banyuls, and Chimienti et al., this volume). While a number of sites pre-
possibly south of Thassos Island; likewise live D. dianthus sented only patchy or isolated coral occurrences, six areas
was only known from Marseille, from off Euboea Island in have been identified as “CWC provinces” (sensu Taviani
the Aegean Sea, and from Eratosthenes Seamount south of et al. 2011, 2017) due to the dense growth of living corals
Cyprus (Zibrowius 2003; Taviani et al. 2005). (generally interspersed with coral-free sediment patches or
Based on their personal observations and other records accumulations of dead corals): the Bari Canyon, Santa Maria
published by the early 1960s, Pérès and Picard (1964) di Leuca, south Malta, south Sardinia, Gulf of Lions (Catalan-
described the Mediterranean Biocoenose des “coraux Provençal-Ligurian canyons), and Melilla CWC provinces
blancs” (the “white coral” community) as occurring at (Fig. 3.1). The emerging picture is that thriving CWC assem-
depths of at least 300 m on hard grounds that are sufficiently blages that are hotspots of deep-sea biodiversity still occur in
sloped to prevent burial through sedimentation, and the Mediterranean (Taviani, this volume), but have a rather
comprising isolated mounds formed by M. oculata and L. punctuate distribution along the circulation path of the
pertusa, which may be surrounded by depressions where Levantine Intermediate Water (LIW), which appears to be a
mud settles. However, these authors noted that most of the main driver for CWC distribution in the Mediterranean
coral frameworks are actually dead, either entirely or else (Taviani et al. 2017; Chimienti et al., this volume). Whether
with only a few living branches at the top. Pérès and Picard this picture will hold true in the future will ultimately depend
(1964) also noted that the dead “sub-fossil” parts are often on the location of any newly discovered CWC sites, which
buried in muddy sediment, and are associated with a rich will serve to address the still rather fragmentary knowledge
thanatocoenosis of Pleistocene age, whereas the extant on distribution of CWC in the Mediterranean.
biocoenosis is faunally impoverished, especially compared
3 Discovery of Mediterranean Cold-Water Corals 33
Fig. 3.1 Map of the Mediterranean Sea showing the locations of the CWC Province; 3. South Malta CWC Province; 4. Melilla CWC
six cold-water coral (CWC) provinces recognised to date (numbered Province; 5. Gulf of Lions CWC Province; 6. South Sardinia CWC
blue dots: 1. Bari Canyon CWC Province; 2. Santa Maria di Leuca Province)
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A Turbulent Story: Mediterranean
Contourites and Cold-Water Corals 4
Michele Rebesco and Marco Taviani
Abstract 4.1 Introduction

Dynamic bottom current regimes govern cold-water cor-
als as well as contourites. We provide an overview of the The powerful action of deep-water circulation and its ability
general aspects of both research fields, with specific atten- to shape the seafloor is a well-known phenomenon since the
tion to the Mediterranean Sea region, which has the par- sixties (Heezen and Hollister 1964). The resulting sedimen-
ticularity to be a climatically-sensitive mid-latitude tary deposits (named contourites by Hollister and Heezen
semi-enclosed basin. In this area there are many examples 1972) are defined as sediments deposited or substantially
of along-slope contourite deposits (known as contourite reworked by the persistent action of bottom currents (e.g.,
drifts), typically with an along-slope, elongated mounded Stow et al. 2002a; Rebesco 2005, 2014; Rebesco and
shape adjacent to a concave moat. Likewise, a number of Camerlenghi 2008; Rebesco et al. 2014). For “bottom cur-
thriving coral sites, together with sparse occurrences, are rents” it is meant any “persistent” water current near the sea-
present in the central and western Mediterranean, with floor, generally with a net along-slope flow (Fig. 4.1).
large coral mounds known so far only in the Alborán Sea. Contourites were first described in the Atlantic Ocean and
In the Mediterranean Sea both contourite drift and cold- many examples have been discovered also in the
water corals seem mainly related to the Levantine Mediterranean Sea (e.g. Marani et al. 1993; Reeder et al.
Intermediate Water, but their strict co-existence has still to 2002; Roveri 2002; Gaudin et al. 2006; Verdicchio et al.
be ascertained in many cases. Further research should 2007; Verdicchio and Trincardi 2008a, b; Amelio and
address this aspect and the great potential of combining Martorelli 2008; Martorelli et al. 2011; Somoza et al. 2012;
the two complementary kinds of climate paleo-archives Schattner et al. 2015; Pellegrini et al. 2016; Ercilla et al.
provided by cold-water corals and contourites. 2016; Miramontes et al. 2016). The general understanding
regarding contourites is steadily improving with increasing
Keywords recognition that contour currents are major transport and
Cold-water corals · Contourites · Mediterranean Sea · sedimentary processes exerting control on deep-sea sedi-
Bottom currents · Suspended matter mentation (Camerlenghi et al. 1997; Giorgetti et al. 2003;
Rebesco and Camerlenghi 2008). The progress in the knowl-
edge on these deposits confirms their importance, especially
in the fields of paleoclimatology and paleoceanography,
slope-stability, geological hazard assessment, and hydrocar-
bon exploration. Contourite areas are associated with a num-
ber of oceanographic processes at different water depths,
from abyssal plains to continental shelves (Rebesco et al.
M. Rebesco (*) 2014). Such processes include, but are not limited to, dense
OGS, Trieste, Italy
bottom currents, tides, eddies, deep- sea storms, internal
waves and tsunamis.
M. Taviani
Sustained currents significantly affect the seafloor (result-
Institute of Marine Sciences (ISMAR-CNR), Bologna, Italy
ing in large-scale depositional and erosional contourite fea-
tures). Though there is consensus about the large-scale,
Woods Hole, MA, USA
geophysical characteristics of these deposits, the small-scale

https://doi.org/10.1007/978-3-319-91608-8_4
36 M. Rebesco and M. Taviani
Fig. 4.1 Schematic diagram summarising the principal bottom-current features. (Modified from work by Stow et al. (2008); with permission from
© Elsevier)
contourite facies still lack unambiguous and commonly The Mediterranean is a concentration basin with evapora-
accepted diagnostic criteria, also for distinguishing them tion exceeding the joined effect of river runoff and precipita-
from turbidite facies and bottom-current reworked sandy tion (Skliris, this volume). The circulation is strongly
deposits (Rebesco et al. 2014). Most contourite researchers influenced by Atlantic inflow water and by the presence of
consider extensive bioturbation as the dominant feature (e.g. shallow sills (Miller 1972). In general, modern circulation is
Gonthier et al. 1984; Stow and Faugères 2008). However, a anti-estuarine, with a cell in the western Basin and one in the
minority of workers interprets some distinctly laminated eastern Basin (Lascaratos et al. 1999; Robinson et al. 2001).
sandy deposits as contourites (Hüneke and Stow 2008; The relatively fresh and light Mediterranean Surface Water
Martín-Chivelet et al. 2008; Shanmugam 2008, 2013; Mutti (MSW), entering from the Atlantic, occupies the upper tens
and Carminatti 2012). In those regions of the ocean suitable of m and interchanges with the salty and relatively warm
for cold-water coral (CWC) settlement, bottom currents are Levantine Intermediate Water (LIW; Wüst 1961; Fig. 4.2),
also steadily or periodically delivering food particles to which forms southeast of Crete, in the eastern Mediterranean
sessile suspension-feeders and limit excess silting. A link Basin (Millot 2009; Pinardi and Masetti 2000; Hecht et al.
between contourites and CWCs has been noticed in the Gulf 1988; Rubino et al. 2012; Bensi et al. 2013).
of Mexico (Hübscher et al. 2010), and the distribution of
contourites in shallow to intermediate depths may provide a
first order indication for the presence of CWCs and vice 4.3 Contourite Deposits
versa (Hebbeln et al. 2016).
We discuss the action of dynamic bottom current regimes In the Mediterranenan Sea there are many examples of
with relation to contourites and CWCs by providing a general along-slope contourite deposits, known as contourite drifts,
overview, with a particular attention to the Mediterranean (Verdicchio and Trincardi 2008a). They are mostly located at
Sea region. intermediate water depths (about 200–600 m) and associated
with the LIW (e.g. Marani et al. 1993; Reeder et al. 2002;
Roveri 2002; Gaudin et al. 2006; Verdicchio et al. 2007;
4.2 Hydrographic Setting Verdicchio and Trincardi 2008a, b; Amelio and Martorelli
2008; Martorelli et al. 2011; Somoza et al. 2012; Schattner
The Mediterranean Sea is a semi-enclosed basin, character- et al. 2015; Pellegrini et al. 2016; Ercilla et al. 2016;
ised by moderate-energy continental margins and micro- Miramontes et al. 2016). Normally, these relatively shallow
tidal conditions, that communicates with the Atlantic Ocean water contourite drifts (Fig. 4.3) are similar (either in terms
through the narrow Strait of Gibraltar (Robinson et al. 2001; of shape in plan-view and of internal geometry) to the better
Hayes et al., this volume). known oceanic counterparts (Verdicchio and Trincardi
4 A Turbulent Story: Mediterranean Contourites and Cold-Water Corals 37
Fig. 4.2 Map of the Mediterranean Sea showing a simplified scheme are identified by numbers: 1 = Bari Canyon; 2 = Santa Maria di Leuca;
of water circulation with respect to Levantine Intermediate Water 3 = South Malta; 4 = Melilla; 5 = Gulf of Lion; 6 = South Sardinia. Red
(LIW) and deep water. Rectangles indicate areas with contourite dots refer to minor occurrences of live CWC. (Modified from Taviani
deposits discussed in the text. Main cold water coral (CWC) provinces et al. 2016. With permission from © Elsevier)
a b
TWT W
(msec) –200 Simple drift
675
–509 m SD (m)
M
–532 m –350
deposit
725
truncated
E –500
reflectors –568 m
–650
775 US MS
20 m
bottom current
825 toward the reader
1000 m
Seismic line YD205
Fig. 4.3 Bottom-current deposit along the slope of the SW Adriatic the relationship between bottom-current deposits, erosional areas,
Margin. (a) Chirp-sonar profile showing a separated drift (SD) rimmed, changes in slope gradient and seafloor roughness. (From Verdicchio and
upslope, by a well-defined moat (M). (b) Schematic representation of Trincardi (2006); with permission from © Elsevier)
2008a). In fact, bottom currents are known to construct large bottom-water circulation, Mediterranean contourite drifts
accumulations of sediments which vary greatly in location, are generally smaller in size and encompassing a shorter
morphology, size, sediment patterns, construction deposition interval.
mechanisms and controls (Faugères and Stow 2008). In addition, various depositional and erosional bedforms
Typically, contourite drifts have an along-slope, elongated are generated by bottom currents (Stow et al. 2013). They are
mounded shape, and an adjacent concave moat (Rebesco and highly variable in terms of sediment composition, morphol-
Stow 2001). The oceanic drifts (Fig. 4.4) can be more than ogy and dimension, from decimetres to kilometres (Wynn
100 km wide, several hundreds of kilometres long, up to and Masson 2008). The detection of bedforms can be impor-
2 km thick and have a relief of up to 1.5 km (Rebesco et al. tant for the reconstruction of bottom-current velocity
2014). Their areal extension ranges from ca. 100 km2 (small (Fig. 4.5) in absence of direct oceanographic measurements
patch drifts) to >100,000,000 km2 (giant elongated drifts). (Stow et al. 2009). Contourite deposits vary widely in their
As a consequence of shallow water margin physiography and lithology, grain size and composition (Shanmugam 2006,
Fig. 4.4 Schematic model showing ideal, large-scale characteristics of oceanic contourite drifts and channel-levee systems. (From Rebesco
et al. (2014); with permission from © Elsevier)
Fig. 4.5 Bedform-velocity matrix for deep-water bottom current sys- The matrix was obtained using a large amount of data and has a general
tems, showing a schematic representation of bedforms in function of validity for all marine basins, including the Mediterranean Sea. (From
mean grain size of sediment versus flow velocity at or near the seafloor. Rebesco et al. (2014); with permission from © Elsevier)
Fig. 4.6 Examples of the a Bigradational sequences b Base-cut-out type d Sandy contourites
principal sedimentary facies
Gradational
for the contourites recovered contact
10 cm
Normal grading
during IODP Expedition
Calcareous mud
Laminations
Silty mud
Sand, silty sand and sandy silt interbeded with silty mud
339 in the Gulf of Cádiz
10 cm
under the influence of the
Mediterranean Outflow Water
(MOW). (From © Hernández-
10 cm
Sandy mud
Molina et al. (2013))
biogenic carbonate biogenic carbonate biogenic carbonate

Silty mud with
Laminations
Bigradational grading
Laminations
Sandy mud with

339-U1390A-8H-6A
Irregular
contact
c Top-cut-out type 339-U1388B-20X-5A
Silty mud with
Sandy mud
10 cm
Inverse grading
Calcareous mud
Silty mud
339-U1390A-8H-6A
339-U1388C-3R-2A
2013; Stow et al. 1996, 1998, 2002b; Stow and Faugères CWCs, as sessile suspension feeders, depend on bottom cur-
2008). Most bottom-current deposits show a characteristically rents delivering food particles (Frederiksen et al. 1992;
mixed composition, including biogenic, terrigenous, White et al. 2005; Duineveld et al. 2007). In fact, the likeli-
volcanoclastic and authigenic components (Stow et al. 2008). hood for a coral to catch food particles sinking through the
Most commonly, contourite deposits (Fig. 4.6) are rather water column (Fig. 4.8) is appreciably enhanced when their
poorly sorted, mud-rich, intensively bioturbated, interlay- trajectory is sub-horizontal in response to the action of a
ered with thin fine-grained sandy/silty beds, and show a cer- sideways bottom current flow (Dorschel et al. 2007; Davies
tain kind of rhythmic stripes (Stow et al. 2002b). Less et al. 2009). Furthermore, if persistent over time, they also
commonly, sandy contourite deposits have been reported, help promoting soft sediment induration and lithification
e.g. in the Gulf of Cádiz (Hanquiez et al. 2007; Hernández- turning into firm and hardgrounds thus producing substrates
Molina et al. 2014). Finally, both sandy and muddy contou- eventually suitable for coral colonisation (Allouc 1990;
rite deposits are relatively frequently associated with CWC Remia et al. 2004; Toscano and Raspini 2005; Noé et al.
habitats (Fig. 4.7; Huvenne et al. 2009; Savini and Corselli 2006; Conti et al. 2013). Finally, currents may act as con-
2010; Martorelli et al. 2011; Van Rooij et al. 2011; Henriet veyor belts for the coral propagules ensuring their dissemi-
et al. 2014; Hebbeln et al. 2015, 2016). nation over long distances (Henry et al. 2014). As a matter of
fact, prospering CWCs are mostly linked to a vigorous bot-
tom water regime (Van Rooij et al. 2007b; Freiwald et al.
4.4 Currents and Ecosystemic Response 2004, 2009; Hebbeln et al. 2014, 2016; Wienberg and
Titschack 2017; Taviani et al. 2016).
Both contourites and CWCs are dependent from hydrodyna- Contourites and CWCs are often found in association
mism. Bottom currents are, in fact, one important factor con- when subject to dynamic current regimes in shallow to inter-
trolling deep-water ecosystems, including CWCs (Van Rooij mediate water depths. In the Atlantic Ocean, Hebbeln et al.
et al. 2007a; Huvenne et al. 2009; Hebbeln et al. 2016).The (2016) found a clear relationship between contourite sedi-
Fig. 4.7 PARASOUND
profile across the western rim
of the West Melilla Cold-
Water Coral Province
showing a sediment drift
(sampled in core GeoB
18131-1) adjacent to a
Cold-Water Coral mound
structure (sampled in core
GeoB 18130-1). Further to
the east a buried Cold-Water
Coral mound also appears.
(From © Hebbeln et al.
(2015))
Fig. 4.8 Cold-water coral (CWC) and bottom current interaction. ticles to be caught by a coral with increasing bottom currents (green
(a–c) CWC framework showing the transition from the living part of arrows) and (ii) the baffling effect of the CWC framework on sus-
the CWC colony growing on top of dead coral framework. See exam- pended sediment particles transported along with the bottom currents
ples from the Irish margin (a) and the Campeche margin off Mexico (b (brown arrows). (From Hebbeln et al. (2016) with permission from ©
and c). (d) Sketch indicating (i) the increasing probability of food par- Elsevier)
median (µm) δ18O (%o PDB) (Montagna et al. 2006; McCulloch et al. 2010; Fink et al.
0 5 10 15 20 25 4 3 2 2012, 2015). A combined analysis of associated contourites
a b corals
0 +
and CWCs may provide the opportunity for a comprehensive
Holocene
+ understanding of past changes in both climatic and environ-
+
+
+
+ mental conditions (Hebbeln et al. 2016).
+
100 +
–
–
–
–
– 4.5 CWC Establishment
core depth (cm)
–
–
200 –
–
– Twenty years plus of research devoted to the study of CWC
–
– in the Mediterranean basin permits a comprehensive over-
Late Weichselian
–
–
–
–
view of the main traits of CWC spatio-temporal colonisation
300 –
– in this basin. At present, a number of healthy CWC sites have
–
–
– been identified in the central and western Mediterranean
– (Southern Adriatic, Northern Ionian, Strait of Sicily, South
–
400 –
–
– Sardinian, Ligurian-Provencal-Catalan canyons, Alborán),
– together with sparse occurrences (Freiwald et al. 2009;
–
~30 kyr –
– Orejas et al. 2009; Vertino et al. 2010; Savini et al. 2010,
–
500 –
2014; Taviani et al. 2011a, 2015, 2016; Madurell et al. 2012;
GeoB 6718-2 GeoB 6718-2 Gori et al. 2013; Angeletti et al. 2014; Fanelli et al. 2017;
Fig. 4.9 Example of relationship between contourites and coral growth
Wienberg and Titschack 2017; Altuna and Poliseno, this vol-
on the Irish margin. (a) Median grain-size (showing a Holocene ume; Chimienti et al., this volume; Vertino et al., this vol-
bigradational grading typical of contourite facies; orange arrows) and ume). The major CWC provinces (sensu Taviani et al. 2011a)
stable oxygen isotope data (core GeoB 6718–2 in a contourite setting appear to be on the main track of the LIW (Freiwald et al.
close to Propeller Mound, Porcupine Seabight, Dorschel et al. 2005).
(b) Regional pattern of the temporal occurrence of cold-water corals
2009; Fink et al. 2015; Taviani et al. 2015, 2016).
along the Irish margin (Frank et al. 2011) with coral growth likely The current knowledge suggests that substantial CWC
linked to Holocene strong bottom currents, as shown by increased growth took place in the Mediterranean since the Pliocene,
grain-size in (b). (From Hebbeln et al. (2016) with permission from © after the Messinian Salinity Crisis (Taviani et al. 2005a;
Elsevier)
Vertino et al. 2014, this volume; Freiwald, this volume).
Extant CWC of Atlantic affinity (i.e., the highly emblematic
mentation and CWCs during the Holocene (Fig. 4.9). Of Lophelia pertusa, Madrepora oculata, Desmophyllum dian-
course, this is true below a certain flow velocity threshold, thus) are widespread in the basin since the middle Pleistocene
but when the bottom current circulation becomes too at least, but their spatio-temporal occurrence, persistence or
vigorous it starts to be erosive and destructive. Contourites decline in the Mediterranean is marked by regional or local
are, however, much more widespread than CWC occurrences circumstances. For instance, such CWC displayed a basin-
since the latter are dependent also from productivity in addi- wide distribution during the late Pleistocene that included
tion to dynamic current regimes. the eastern Basin (Taviani et al. 2011b), but then suffered
On the one hand, contourites facies, inferred to reflect important regional setbacks driving to their decline or
long-term changes in the bottom current strength (Stow and demise. Climatically-driven factors evoked to have impacted
Faugères 2008), are valuable high-resolution paleo-archives on Mediterranean CWC survival are silting (Remia and
of climate and environmental changes (Viana and Rebesco Taviani 2005; McCulloch et al. 2010), nutrients (Montagna
2007; Rebesco et al. 2014). On the other hand, the aragonitic et al. 2006) oxygen (Fink et al. 2012), temperature
coral skeleton is equally archiving relevant (McCulloch et al. 2010), productivity (Fink et al. 2013) or
palaeoceanographic information, which can be decoded their interaction. Whatever is backing the past, present and
through opportune geochemical techniques (Cheng et al. future history of Mediterranean CWC, one basic tenet is the
2000; Adkins et al. 2003; Rüggeberg et al. 2008; Montagna role of oceanography, what includes the whole current
et al. 2005, 2011, 2014; López Correa et al. 2010; McCulloch system that is not stable over time since responding to
et al. 2012; Robinson et al. 2014; Montagna and Taviani, this climatic forcers. Sortable silt particle-size data reveal that the
volume). In fact, the application of precise U-series and 14C Mediterranean intermediate circulation fluctuated on
dating to Mediterranean CWC, and trace and minor element Milankovitch to millennial time-scales between cold / faster
geochemistry has already allowed to disclose major (and well-ventilated and deepening) at time of climate
variations in their distribution and paleoceanographic degradation (Toucanne et al. 2012). The development of
contour current conditions in the late Pleistocene to present contourite drifts in the Tirrenian and Ionian seas was
enhanced after the Middle Pleistocene Transition (700–900 However, corals like M. oculata and D. dianthus have been
kyr) (Miramontes et al. 2016; Rebesco et al., in prep). The documented also outside the canyon system itself as sparse
LIV velocity changed in the past with faster bottom currents occurrences on hardgrounds and other suitable substrates
and greater accumulation of fine sediment during cold under the influence of strong bottoms currents (Freiwald
periods and sea level low stands (Miramontes et al. 2016). et al. 2009).
Neodymium isotopic composition record from intermediate Although it has been highlighted the positive feedback of
depths in the western Mediterranean Sea supports a vigorous currents, that account for contourites and concomitantly
deep overturning with a decrease of the deep-water intensity sustain coral growth, it should be contemplated that actively
afterward (Dubois-Dauphin et al. 2017). Also suggests that drifting sediment may also cause their ultimate burial if
at about 8.7 ka BP western-sourced intermediate water likely established on their trajectory.
replaced LIW that was no longer produced (or heavily
reduced) in the eastern basin, potentially supporting a
reversal of the Mediterranean circulation. 4.6 Conclusions and Future Perspectives
Coral mounds in the Mediterranean are often represented
by small-relief expressions, probably one or few generations Contourite drift occurrences and major CWC provinces in
of coral growth, or by the colonisation of pre-existing the Mediterranean Sea appear to be largely controlled by the
‘mounded’ features. This is the case of CWC growth at Santa LIW. However, much is still to be understood since both
Maria di Leuca CWC province in the northern Ionian Sea, fields of research are relatively young for the Mediterranean
where M. oculata and L. pertusa settle over submarine- Sea, dating back to some 15 years. Further discoveries are
slumped blocks (Taviani et al. 2005b; Savini and Corselli hence expected regarding the likely co-occurrence of
2010; Savini et al. 2016; Bargain et al. 2017), or in the contourites and CWCs, and here is where further research is
southern Adriatic Sea (Freiwald et al. 2009) and Alborán Sea motivated.
(Wienberg, this volume). Larger features (tens to hundreds It is predictable that substantial CWC growth is present in
meters thick) coral mounds are known at various sites in the the area of the Corsica Channel where sediment drifts
Atlantic Ocean (Reed 2002; Kenyon et al. 2003; van Weering presence has been documented by Roveri (2002). Although
et al. 2003; Mienis et al. 2007; Wheeler et al. 2006, 2011; not much CWC evidence has been produced thus far,
Hebbeln et al. 2015, 2016; Wienberg and Titschack 2017). Madrepora oculata does occur indeed alive in the area
They are, however, uncommon in the Mediterranean Sea (M. Taviani, unpublished data), together with now-buried
(Wienberg and Titschack 2017; Taviani et al., this volume; coral mounds (Remia and Taviani 2005). The Strait of Sicily
Wienberg, this volume). The closest example of Atlantic- is another area that deserves to be investigated in-depth for a
type large mounds in the Mediterranean is found in the potential relationship between sediment drift and CWC
Alborán Sea (Hebbeln et al. 2009, 2015; Fink et al. 2013; Lo (Martorelli et al. 2011).
Iacono et al. 2014; Stalder et al. 2015; Wienberg and The LIW glacial-interglacial variability, observed in sedi-
Titschack 2017). Factors controlling the aggradation of large mentary core records (Toucanne et al. 2012; Miramontes
coral mounds have been reviewed by Wienberg and Titschack et al. 2016; Dubois-Dauphin et al. 2017) documenting better
(2017) but some aspects still need to be explored in greater ventilation and faster bottom water mass movement in cooler
detail in the future. Regarding a strict connection between times with respect to the early Holocene, provides fertile
contourites and CWC in the Mediterranean, it can be ground to explore potential responses of CWC as well.
observed that a spatial relationship seems to date ascertained Finally, the paleo-climate archives included in contourites
only at some sites. One clear example is that of the Melilla and in CWC are synergic and both respond to oceanographic
CWC Province where clusters of CWC mounds are regimes driven by climatic forcing. Further research should
associated with sediment drifts and contourite moats hence address the match between the complementary
(Hebbeln et al. 2015, Fig. 4.7). Another case is for example information provided by the two different paleo-archives.
that of the southwestern Adriatic Sea whose seabottom is
profoundly impinged by bottom currents. A number of Acknowledgements Thanks are due to Eleonora Martorelli and Dirk
impressive bedforms is documented there at bathyal depths, Hebbeln for their critical comments that helped improving the clarity of
the text. This chapter is part of EU CoCoNet project, (contract no.
encompassing mudwave fields, barcans and sediment drift 287844) EVER-EST Horizon 2020 project (contract no. 674907), DG
mounds (Trincardi et al. 2007; Foglini et al. 2016). The area Environment programme IDEM (grant agreement No 11.0661
is site of important coral growth and comprehends the Bari /2017/750680/SUB/EN V.C2), and Flag Project Ritmare Ricerca
Canyon CWC province thought to be influenced by the North Italiana per il Mare). Ismar-Bologna scientific contribution n. 1917.
Adriatic Dense (or Deep) Water (Taviani et al. 2015).
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Drop Chapter
Messinian Salinity Crisis: What 5
Happened to Cold-Water Corals?
André Freiwald
Abstract Introduction
The fate of bathyal coral communities prior, during and
after the environmentally devastating Messinian Salinity The fate of cold-water corals (CWC) thriving in bathyal
Crisis is briefly reviewed. The Messinian Salinity Crisis environments during the advent of the Messinian Salinity
has created a geologically short-termed but massive dis- Crisis (MSC) is poorly constrained and deserves apprecia-
ruption to marine life in the Late Miocene Mediterranean tion. The MSC represents an extraordinary and extreme
Sea. First signs of deteriorating environmental conditions event that affected the whole Late Miocene Mediterranean
begun about 7.15 Ma ago with a successive reduction of Sea by the deposition of more than a million cubic kilome-
water mass exchange between the open Atlantic Ocean ters of salt within probably less than 700 ka (CIESM 2008;
the Mediterranean Sea and progressively diminishing Roveri et al. 2014a). Main trigger was a tectonically-driven
deep-water ventilation in the remaining Mediterranean continuous restriction of water exchange with the Atlantic
basins. The resulting deposition of three massive evapo- Ocean through the former Betic and Rifean corridors, added
rite sequences causes a vivid debate until today on the by coeval climatic forcings and their feedbacks on sea-level
degree of desiccation ranging from a complete dry-out to fluctuations (Krijgsman et al. 1999). Since the introduction
a much milder course of events in the Late Miocene of the concept of the MSC by Selli (1954), the search for its
marine realm. The sudden marine reflooding via the causes and effects stimulated numerous geologic disciplines
newly formed Gibraltar gateway at 5.33 Ma abruptly ter- and research programs. The usually most considered MSC
minated the ecological crisis and gave way to fully marine scenario implies high-amplitude sea-level oscillations in the
conditions in the Mediterranean Sea. The preservation range of about 1500 m of the Mediterranean Sea up to its
and the fate of bathyal corals during this event is fragmen- complete desiccation (“shallow water – deep basin model”
tary and still understudied. Existing knowledge indicate of Hsü et al. 1973).
that most of the bathyal coral genera and species are pres- However, even after 65 years of intense research, major
ent or re-appeared in the Early Pliocene (Zanclean) and questions remain unsolved and new discoveries open alter-
that major losses in species richness appeared much later native thoughts and views (see Roveri et al. 2014a, b; 2016
during the advent of the Pliocene. and Vai 2016). The cataclysmic MSC paradigm is now chal-
lenged by an alternative scenario which suggests a “milder”
Keywords MSC evolution by assuming the presence of a permanent
Cold-water corals · Messinian salinity crisis · Miocene · water body in the Mediterranean during the entire MSC and
Pliocene · Bathyal the formation of subaqueous evaporite precipitation in the
deep basins (Roveri et al. 2016 for review).
A major obstacle is a still unavailable comprehensive
stratigraphic framework linking the physically disconnected
onshore and offshore sedimentary sequences. Geophysical
A. Freiwald (*) seismic explorations of MSC sequences which are buried
Meeresforschung, Senckenberg am Meer,
Wilhelmshaven, Germany under Plio-Quaternary sediments in the deep basins still
e-mail: [email protected] await precise stratigraphic calibration and correlation
through deep-sea drilling campaigns in the future.

https://doi.org/10.1007/978-3-319-91608-8_5
48 A. Freiwald
The Temporal Sequence of the MSC and species can be traced during the advent of the
Plio-Pleistocene.
The prelude of the Messinian evaporite deposition started In general, bathyal CWC-bearing deposits in the
with the narrowing of the two Atlantic-Mediterranean gate- Mediterranean pre-Messinian are poorly studied and pro-
ways, the Betic and the Rifean corridors, already in the Late vided so far punctuated information only. As today, the
Tortonian. Progressively restricted water exchange and shal- bathyal mud-dominated paleoenvironments provided habitat
lowing depths led to a reduced circulation and a subsequent for mostly solitary CWC, whereas hard substrates facilitated
drop of deep-water ventilation in the Mediterranean short the colonisation of colonial, or potentially constructional,
after the Tortonian-Messinian boundary at 7.15 Ma CWC species.
(Kouwenhoven et al. 2003; Seidenkrantz et al. 2000). Apparently, pre-Messinian CWC peaked in the
Probably enhanced by increasing surface salinities, the cal- Burdigalian-Langhian (20.44 to 15.97 Ma) with more than
careous plankton as well as deep-water foraminifer commu- 30 genera, including the colonial framework constructors
nities experienced a sudden drop in diversity at 6.7 Ma Lophelia, Madrepora and Enallopsammia, known from
(Blanc-Valleron et al. 2002; Kouwenhoven et al. 2003; Sierro bathyal marl deposits of the Turin Hills, northern Italy (sum-
et al. 2003). The following stepwise disruption has led to marised in Vertino et al. 2014 and further references therein,
three differentially developed main stages which character- Fig. 5.1a). A circalittoral to upper bathyal example of a Late
ise the MSC (CIESM 2008; Manzi et al. 2013; Roveri et al. Tortonian CWC occurrence is preserved in the Calcare di
2014a, b, c): First, evaporates precipitated in shallow basins Mendicino of the Amanthea Basin, Calabria, Italy
bordering the deep offshore main basins from 5.97 to (Mastandrea et al. 2002). This coral bank, 5–8 m thick and
5.60 Ma. Second, evaporite deposition progressed towards approximately several hundred meters wide, was constructed
the deepest depocenters and affected the main basins from solely by Oculina and Dendrophyllia and intercalated with
5.60 to 5.54 Ma (Roveri et al. 2016). The third stage started subaqueous dune sands deposited in a vigorous current
in shallow basins with selenite and laminar gypsum evapo- regime of a paleo-strait. Other, poorly known but rich den-
rates (Manzi et al. 2009) followed by a widespread shift to drophyllid coral assemblages are preserved from deeper
the Lago Mare deposits at 5.42 Ma (Roveri et al. 2008), fed water deposits of Serravallian-Tortonian (13.65–7.25 Ma)
by fresh- and brackish water supply from the surrounding age in the Salento area (Vertino, personal communication
Mediterranean hinterland and from Paratethyan seaways. and Fig. 5.1b). The only intra-Messinian example displaying
The restricted-marine Messinian episode terminated abruptly a hard-substrate bathyal CWC environment is preserved in
at 5.33 Ma with the reflooding of the Mediterranean through sedimentary dikes at Carboneras, eastern Betics, Spain,
the newly formed Strait of Gibraltar. This event marked the known as Brèche Rouge (Barrier et al. 1991; Montenat et al.
stratigraphic boundary to the Zanclean series of the Pliocene 2000). These sediment pockets contain a snapshot of a
and brought back fully marine conditions within short time. bathyal CWC assemblage comprising scleractinians
However, there is an increasing body of evidence that marine (Madrepora, Dendrophyllia, Desmophyllum, Caryophyllia,
incursions, indicated by fully marine fishes, already started Javania, Balanophyllia, Flabellum), gorgonians and
along with the Lago Mare during the latest Messinian stylasterids.
(Carnevale et al. 2006, 2008). This questions a complete iso- Assumingly, along with the progressive reduction of
lation of the Mediterranean basins from marine influx during deep-water ventilation in the Mediterranean basins due to a
the whole course of the MSC and argues for at least periodi- disruption of water exchange with the Atlantic, the fidelity
cal connections to the open ocean (Roveri et al. 2014b; Vai and diversity of benthic organisms became negatively
2016). affected by the spread of stagnant and oxygen-poor deep
water conditions. In some basins, the lack of deep-water
oxygenation gave way to the deposition of euxinic black
The Impact of MSC on CWCs shales during the advent of the MSC. Such a devastating evo-
lution that has fostered the local extinction of benthic life is
Several authors have analysed the broad-scale fossil record documented in the hemipelagic Sant’Agata Fossili
of scleractinian corals including those which thrived in Formation, a bathyal mud paleoenvironment from the
bathyal depths from Miocene to Pleistocene peri- Piedmont Basin (Corselli 2001; Dela Pierre et al. 2011).
Mediterranean outcrops and associated museum collections Even under the assumption of a permanent water body
(Corselli 2001; Taviani et al. 2005; Vertino et al. 2014, this scenario during the MSC in the Mediterranean (see Roveri
volume). The generic diversity of CWC show no significant et al. 2016), available seawater chemistry data based on
changes when comparing pre-Messinian with Zanclean out- strontium isotopes (Flecker et al. 2002; Roveri et al. 2014c)
crops, whereas a more pronounced decline of CWC genera show at least during the second and third MSC stages a
5 Messinian Salinity Crisis and Cold-Water Corals 49
Fig. 5.1 (a) Madrepora oculata of Early-Middle Miocene Miocene (Serravallian-Tortonian) age from Salento Peninsula, Italy
(Burdigalian-Langhian) age from Baldissero, Turin Hills, Italy (identi- (identified by A. Vertino from the University of Modena & Reggio
fied by A. Vertino from the Museum of Natural History Collection, Emilia Collection). (Images courtesy of © Agostina Vertino)
University of Torino). (b) Dendrophyllid rudstone of Middle-Upper
strong decoupling from open-Atlantic water (5.60–5.33 Ma), Blanc-Valleron MM, Pierre C, Caulet JP, et al (2002) Sedimentary,
thus limiting a survival window for bathyal CWC consider- stable isotope and micropaleontological records of paleoceano-
graphic change in the Messinian Tripoli formation (Sicily, Italy).
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petroleum systems. Pet Geosci 22:283–290 bution of Mediterranean cold-water corals
Drop Chapter
Did Quaternary Climate Fluctuations 6
Affect Mediterranean Deep-Sea Coral
Communities?
Agostina Vertino and Cesare Corselli
Abstract The Mediterranean is a marginal sea with limited communi-

Despite our limited current knowledge on fossil cation with the Atlantic Ocean. Due to its small volume to
Mediterranean deep-sea corals, data collected so far hint surface area ratio, and being confined between continents, it
at a strong influence of climate modifications on the dis- is much more responsive to climate change than the open
tribution and diversity of these organisms through the ocean (Rohling et al. 2009; Schroeder et al. 2017). Recent
Quaternary. Several species still living in the North projections reveal that significant changes in the
Atlantic became extinct in the Mediterranean Sea at the Mediterranean region climate (warming between 1.5 and
Pleistocene-Holocene boundary, and the highest cold- 2 °C and decrease of precipitation of about 5%) might hap-
water coral mound accretion rates known so far occurred pen in the next few decades (Gualdi et al. 2013) threatening
during the last deglacial phase. Thermal variations of the highly diverse ecosystems of this “miniature ocean”
deep-sea waters have certainly affected distribution and (UNEP 2010, Marbà et al. 2015; Maier et al., this volume;
survival of the most stenothermic coral species. However, Movilla, this volume). Similar phenomena, at variable time-
changes in other environmental variables (such as current scale and magnitudes, occurred also through the geologic
intensity, food supply and sediment rate, oxygenation), history of the Mediterranean Sea, inducing remarkable pale-
influenced by climate forcing, seem to have highly con- oceanographic modifications (e.g., Rohling et al. 2009;
tributed to the decreased diversity of deep-sea corals and Abrantes et al. 2012; Rogerson et al. 2012). As highlighted
reduced accretion rate of coral mounds through the by several authors, climate changes combined with the com-
Quaternary. In order to precisely correlate the observed plex tectonic evolution of this basin strongly influenced com-
modifications of paleoassemblages with climate fluctua- position and spatial distribution of shallow- and deep-sea
tions, additional research effort needs to be conducted on benthic ecosystems in the last million years (e.g., Di
both emerged and submerged coral deposits. Geronimo et al. 1996; Corselli 2001; Taviani 2002; Emig
and Geistdoerfer 2004; Hayward et al. 2009, Monegatti and
Keywords Raffi, 2010; Sabelli and Taviani 2014; Vertino et al. 2014;
Deep-sea corals · Mediterranean · Quaternary · Chefaoui et al. 2017; Freiwald, this volume).
Paleoclimate · Basin-scale extinction The Mediterranean geological record provides clear evi-
dence that the deep-sea coral fauna was severely affected by
palaeoceanographic modifications through the Quaternary
(Di Geronimo 1979; Zibrowius 1987; Vertino 2003; Di
Geronimo et al. 2005; Stalder et al. 2015; Fink et al. 2015;
A. Vertino (*) Moissette et al. 2017; Vertino et al., this volume; Wienberg,
this volume; Titschack, this volume). However the triggering
Department of Earth and Environmental Sciences, Milano-Bicocca
University, Milan, Italy factors that led to the flourishing and decline phases of these
organisms are still under study.
Department of Geology, Renard Centre of Marine Geology, Ghent
University, Ghent, Belgium The current coral fauna of the Mediterranean Sea can be
e-mail: [email protected] considered as an impoverished North Atlantic fauna, espe-
C. Corselli cially in the deep-sea (Zibrowius 1980, Altuna and Poliseno,
CONISMA Local Research Unit (LRU) of Milano-Bicocca, this volume). Focusing on the order Scleractinia, almost all
Department of Earth and Environmental Sciences, Milano-Bicocca known species (33) live also in the NE Atlantic but only 12
University, Milan, Italy

https://doi.org/10.1007/978-3-319-91608-8_6
52 A. Vertino and C. Corselli
Fig. 6.1 (a) Number of

Mediterranean scleractinian
coral species (from
circalittoral to bathyal
environment or exclusively
bathyal), as known so far, in
the Early Pleistocene
(Calabrian stage: Cal), in the
Late Glacial epoch (LG, data
to be confirmed) and in the
modern sea (R: Recent). Red
rectangle: psychrospheric
species. (b-c) The
psychrospheric species
Caryophyllia coronata (=
Caryophyllia sarsiae) from
(b) Early Pleistocene,
Messina (southern Italy) and
(c) the modern NE Atlantic,
Porcupine Seabight (POS
316_525, 1039 m water
depth). (Photographs ©
Agostina Vertino)
and 7 species are known alive at depth higher than 200 m in sentatives of the genera Stephanocyathus, Fungiacyathus,
the western and eastern Mediterranean, respectively, and Deltocyathus, Flabellum and the subgenus Caryophyllia
among them only 4 (3 in the E Mediterranean) are exclusive (Ceratocyathus), and hard-bottom taxa, such as Caryophyllia
to bathyal biocoenoses. A similar trend can be observed in coronata, Seguenza 1864 (= Caryophyllia sarsiae, Zibrowius
other skeletonised coral groups, such as the octocoral fami- 1980) (Fig. 6.1b-c) and Enallopsammia scillae (Seguenza
lies Coralliidae and Isididae and the hydrozoan Stylasteridae. 1864) (= Enallopsammia rostrata, Pourtalès, 1878). The for-
Each is represented by a single species in the modern mer were living on clay- to silt-dominated seafloors and repre-
Mediterranean (Corallium rubrum, Isidella elongata and sent the highest number of extinct species, the latter colonised
Errina aspera) but is much more diverse in the bathyal envi- instead fault escarpments, large boulders or were associated to
ronments of the NE Atlantic (see Altuna and Poliseno and CWC bioconstructions dominated by the species L. pertusa
references therein, this volume). (Vertino 2003; Di Geronimo et al. 2005; Taviani et al., this
Richer Atlantic-like deep-sea coral communities were volume). Over 70% of the Early Pleistocene Mediterranean
instead flourishing in the Early Pleistocene Mediterranean, as deep-sea species live today in NE Atlantic seafloors (Fig. 6.2a)
shown by fossil deposits cropping out along the coasts of the and many of them are “psychrospheric” taxa, i.e. exclusively
Messina Strait (MS) (Vertino 2003; Di Geronimo et al. 2005), known in very deep marine environments at water temperature
recently ascribed to the Calabrian stage (Di Stefano and lower than 10 °C (Fig. 6.1a). Instead ~ 60% of these species
Longhitano 2009), and the island of Karpathos (Moissette (including all psychrospheric taxa) are absent in the modern
et al. 2017). The MS coral buildups, dominated by Lophelia Mediterranean (Figs. 6.1a and 6.2a).
pertusa, and mud-dominated “inter-mound” deposits hosted The increased severity and duration of climate oscilla-
several species extinct in the modern Mediterranean. tions since the mid-Pleistocene transition (Head and Gibbard
Considering only the representatives of the phylum Cnidaria 2005; Capotondi et al. 2016), (2) the (quasi-) periodical
ascribable to bathyal environments, at least 6 species belong- sapropel formation and related dysoxic to anoxic conditions
ing to the above mentioned Isidiidae, Coralliidae and in the eastern Mediterranean deep-sea floors (Rohling et al.
Stylasteridae families, and 14 scleractinian species that were 2015) and (3) the Heinrich and the Dansgaard–Oeschger
thriving on deep-sea Pleistocene seafloors are absent in the stadial and interstadial events of the Late Pleistocene (Cacho
modern Mediterranean (Fig. 6.1a). Among these species it is et al. 2002, 2006; Morabito et al. 2014 with references) had
worth mentioning both typical soft-bottom taxa, such as repre- certainly a profound effect on the Mediterranean deep-sea
6 Quaternary Climate Fluctuations and Deep-Sea Corals 53
Fig. 6.2 (a) Percentage of

deep-sea scleractinian coral
species known in Early
Pleistocene deposits from
Italy and Greece, still living
in the Mediterranean (M) and
in the North-East Atlantic
(NEA). (b) Percentage of
deep-sea species, known thus
far in the Mediterranean
during the Late Glacial
Epoch, still living in the
Mediterranean (M) and in the
North-East Atlantic (NEA)
benthic biota. However, due to the current lack of knowledge Sciuto 2012; Borghi et al. 2014). Several authors have related
of post-Calabrian deep-sea paleocommunities until the last the reduction until the basin-scale extinction of Pleistocene
50 kyr BP (McCulloch et al. 2010; Fink et al. 2015; Vertino Mediterranean psychrospheric species to the remarkable tem-
et al., this volume), robust hypotheses on the impact of perature increase after the Younger-Dryas period and the
Quaternary climate oscillations on deep-sea coral diversity establishment of the current homothermal conditions in deep-
and spatial distribution cannot be drawn. What is known so water environments (e.g., Di Geronimo et al. 1996; Corselli
far is that (1) at least around 60% of the deep-sea Calabrian 2001; Taviani 2002). However, temperature modification can-
species were still present in the basin until the “late glacial” not be considered as the only cause of the deep-sea fauna
(LG) epoch,1 (2) over 90% of the LG species are still living impoverishment at the Pleistocene-Holocene transition. In
in the NE Atlantic (Fig. 6.2b) and (3) almost half of them are fact, it would not explain the disappearance from the
known only as fossils in the Mediterranean (Fig. 6.2b). Mediterranen of less stenothermic Atlantic species, such as S.
Moreover, LG scleractinians include around 30% of Atlantic fissilis and E. cornucopia, that could tolerate temperature of
species (such as Schizocyathus fissilis, Flabellum around 13 °C (Zibrowius pers. comm.).
macandrewi, Eguchipsammia cornucopia) that have not Concerning Mediterranean frame-building cold-water
been found in Early Pleistocene deposits thus far. coral (CWC) species, the modern cosmopolitan distribution
When and why all psychrospheric species disappeared of the most common species (Cairns et al. 1999) and their
from the Mediterranean is not clear yet. The narrow thermal persistence in this basin since the Neogene (Vertino et al., this
range tolerated by these organisms today lead us to hypothe- volume), hint at a their rather high tolerance for environmen-
sise that lower temperatures than 13–14 °C, typical of modern tal changes. Nevertheless, recent experimental studies
Mediterranean bathyal seafloors, occurred both during the focused on L. pertusa, Madrepora oculata and Dendrophyllia
Calabrian stage and the Late Glacial period. This hypothesis cornigera have highlighted the sensitivity, and above all, the
is supported by the modern thermal range of other species species-specific physiological response of these organisms to
(also extinct in the Mediterranean) belonging to molluscs, sudden thermal modifications. D. cornigera seems to be more
bryozoans, polychaetes, crinoids and ostracods found associ- tolerant to temperature increase (Naumann et al. 2013; Gori
ated to the Pleistocene psychrospheric scleractinians (e.g., Di et al. 2014, 2016) than L. pertusa (Brooke et al. 2013) and the
Geronimo et al. 1996, 2005; Rosso and Di Geronimo 1998; latter species appears to acclimate better to low temperatures
(< 10 °C) than M. oculata (Naumann et al. 2013, 2014). These
The total number of species ascribed herein to the “LG epoch” derives
1
results are consistent with the spatial distribution of the three
from literature and must be confirmed. It includes species whose skel- species through the Quaternary. At present, M. oculata and D.
etons have been radiometrically dated (Delibrias and Taviani 1985;
McCulloch et al. 2010) but also taxa that have been ascribed to the LG
cornigera characterise Mediterranean lower circalittoral and
period based on the age of the sediment in which they were embedded bathyal bioconstructions, respectively. L. pertusa can co-
(Allouc 1987; Corselli and Bernocchi 1990; Vertino 2003). occur in Mediterranean bathyal habitats but is much more
54 A. Vertino and C. Corselli
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Drop Chapter
A Deglacial Cold-Water Coral Boom 7
in the Alborán Sea: From Coral Mounds
and Species Dominance
Claudia Wienberg
Abstract
The two scleractinian cold-water corals Lophelia pertusa than 2000 m. It has a complex seafloor topography with three
and Madrepora oculata are widely distributed in the sub-basins separated by volcanic ridges and seamounts
Alborán Sea. They have been found (alive and fossil) on (Muñoz et al. 2008). The two prominent framework-forming
seamounts, volcanic ridges and mud volcanoes, and they scleractinian cold-water corals (CWC), Lophelia pertusa
formed coral mounds in the geological past. While the and Madrepora oculata, are widely distributed in the AS
cold-water corals show a reduced occurrence during the comprising living and fossil occurrences (Fig. 7.1a; see also
last glacial period, they experienced a boom since the last Chimienti et al., this volume; Vertino et al., this volume).
deglaciation until the Early Holocene. The proliferation of They are a common member of the faunal community colo-
cold-water corals during this time is expressed in very high nising various seamounts and ridges (Palomino et al. 2015
vertical mound aggradation rates of >400 cm kyr−1. Since and references therein; see Rueda et al., this volume; Lo
the mid-Holocene coral mound aggradation significantly Iacono et al., this volume). They are also associated to a
slowed-down, which is ascribed to the reduced occurrence rather exceptional habitat as they have been encountered on
of cold-water corals likely supplemented by a reduced some of the mud volcanoes within a large mud diapir prov-
sediment supply. During the Holocene, a shift in coral ince in the western AS (Margreth et al. 2011; Palomino et al.
species dominance towards a M. oculata-dominated cold- 2018). However, L. pertusa and M. oculata do not just occur
water coral community becomes apparent. It is speculated as single living colonies or as scattered small-sized accumu-
that in comparison to L. pertusa, M. oculata has a higher lations of coral rubble and dead framework on topographic
tolerance against the increasing Holocene bottom water highs, both species also formed substantial accumulations on
temperatures, but is not efficient in building-up mounds the seafloor, which over thousands of years developed to
likely attributed to its thinly branching framework. mound- or ridge-like seabed structures of tens of metres in
height. Such coral mounds are composed of skeletal rem-
nants of both species (and other benthic organisms) and sedi-
Keywords ments. Their formation depends on a well-balanced interplay
Lophelia pertusa · Madrepora oculata · Deglaciation · between sustained coral growth, the development of a coral
Coral mound · Mound aggradation · Environmental framework with a high sediment baffling capacity, and the
tolerance · Alborán Sea continuous supply of sediments which stabilises the biogenic
construction (Wienberg and Titschack 2017).
In the northern AS, up to 9-m-high mounds grouped into
provinces have been reported from southeast of Málaga and
The Alborán Sea (AS) comprises the westernmost part of the north of the Chella bank in water depths between 150 and
Mediterranean Sea, which is bordered by the Spanish and 250 m (Muñoz et al. 2008). Potential mound structures are
Moroccan continental margins (Fig. 7.1a). The AS is a very also reported from some seamounts (e.g., Herradura, Chella)
narrow basin (180 × 330 km) and water depths are shallower and from the Alborán ridge (Fig. 7.1a; Lo Iacono et al. 2008;
Palomino et al. 2011; Lo Iacono et al., this volume). However,
C. Wienberg (*) all these reports are mainly based on acoustic data and a defi-
MARUM – Center for Marine Environmental Sciences, University nite evidence that these structures are formed by CWC is still
of Bremen, Bremen, Germany lacking. For mounds discovered in the southern AS, it is

https://doi.org/10.1007/978-3-319-91608-8_7
58 C. Wienberg
Fig. 7.1 (a) Bathymetric map of the Alborán Sea (data source: http:// they are not published yet). (b) Complete coral age dataset obtained for
www.emodnet-hydrography.eu) showing its volcanic ridges, seamounts/ L. pertusa and M. oculata collected in the Alborán Sea (note: two
banks (alternative names found in literature are given in brackets), and recently published glacial ages of 28,560 and 43,040 years BP obtained
mud volcanoes. Displayed are reported live/fossil occurrences of for L. pertusa are not displayed, see Dubois-Dauphin et al. 2016). (c)
Lophelia pertusa and Madrepora oculata, coral mounds formed by Separation between L. pertusa (pink) and M. oculata (orange) ages.
both species, and sites from which coral ages are available (note: core Ages that derived from coral mounds and from other habitats are
records from the East Cabliers bank and the West Melilla province are indicated. See legend for symbol code; see text for references. YD
indicated but not considered for the coral age plots shown in b and c as Younger Dryas, BA Bølling-Allerød, LG late glacial period
already proven by video observations and long sediment to curved coral mounds (height: > 20 m) occurs, followed by
cores that substantial parts of these structures have been a cluster with elongated mounds (height: < 20 m) with some
build up by L. pertusa and M. oculata. The East Melilla of them being partly buried by sediments (Hebbeln, this
province comprises coral mounds with different morphologies volume). The West Melilla province, situated 50 km
(Hebbeln, this volume). In the north, steep and elongated westward of the East Melilla province (Fig. 7.1a), comprises
ridges (Brittlestar ridges I to III) are attached to the southern >100 mounds, which are organised in two clusters, occur in
edge of the Provençaux bank (Fig. 7.1a). They have heights water depths of 300–590 m, and have heights of 10–45 m.
of 50–150 m and rise to water depths of 250–450 m (Fink The mounds have an asymmetrical to circular shape and
et al. 2013). Their morphology and orientation might point to some of them are completely buried by sediments (Lo Iacono
a tectonic-related origin, but a recent drilling campaign et al. 2014). No living CWC are found today on these mounds
revealed that at least the upper 70 m of these ridges are made (Lo Iacono et al. 2016). A third coral mound site exists to the
up of coral-sediment-deposits (Hebbeln et al. 2015). Lophelia north of the Melilla provinces on the East Cabliers bank
pertusa and M. oculata still colonise these ridges today (Fig. 7.1a), which is a 25-km-long N-S oriented structurally
though in low numbers and as small and scattered colonies. controlled volcanic ridge. Substantial coral accumulations
To the south at water depths below 300 m, a field with oval have been deposited on the crest of this structure, which rises
7 A Deglacial Cold-Water Coral Boom in the Alborán Sea 59
today to water depths of 250–710 m. In the northern portion, Stalder et al. 2015). Concurrent with the onset of the mid-
living occurrences of L. pertusa and M. oculata were Holocene occurs a relevant gap in the age dataset (Fig. 7.1b).
observed (Lo Iacono et al. 2016). This ~2,500-years-lasting temporary reduced occurrence of
Many efforts have been conducted to gain information CWC was likely related to a significant decrease in produc-
about the past occurrence of L. pertusa and M. oculata in the tivity after 9,000 years BP, which occurred concurrent to the
AS. Until the present day, ~80 datings have been published termination of the organic rich layer deposition in the AS
for both species (Fig. 7.1b). This dataset contains datings (Fink et al. 2015; Cacho et al. 2002). After ~5,800 years BP,
obtained from CWC fragments collected from the seabed sur- CWC seem to be present in the AS until the present-day,
face (n = 35), which mainly originate from seamounts (see except from two gaps at the transition from the mid- to Late
compilation by Fink et al. 2015 and references therein), while Holocene and during the Late Holocene (Fig. 7.1b). Overall,
the majority of ages (n = 47) derive from core records all presently observed age gaps need to be considered with
retrieved from coral mounds along the Moroccan margin care as the lack of dating does not necessarily indicate the
(Fink et al. 2013; Stalder et al. 2015; Dubois-Dauphin et al. complete absence of CWC but clearly document phases of
2016; unpubl. Data Wienberg). Overall, sediment cores col- reduced CWC occurrence in the AS. Moreover, as the
lected from coral mounds are crucial to reconstruct recurring majority of coral ages derive from the East Melilla province,
periods of sustained coral colonisation on these mounds (see it cannot be excluded that the identified temporal pattern
Angeletti et al., this volume), and thus, to identify periods of might slightly differ for other coral sites in the AS.
enhanced vertical mound aggradation under suitable environ- The identified temporal pattern in the general occurrence
mental conditions (Wienberg and Titschack 2017). The num- of CWC in the AS is even more clearly displayed in core
ber of CWC ages obtained for the AS is still rather low but records obtained from individual coral mounds, and is
will potentially significantly increase in the near future with explicitly expressed in the varying vertical aggradation rates
respect to ongoing studies for which more than 100 new dat- estimated for these mounds. Coral mounds of the East
ings are expected for the East and West Melilla provinces, and Melilla province show highest aggradation rates of >400 cm
the East Cabliers bank (Krengel et al. 2015; Lo Iacono et al. kyr−1 for the last deglaciation and up to ~300 cm kyr−1 for the
2016; Wang et al. 2016). However, the available dataset Early Holocene (Fink et al. 2013; Stalder et al. 2015;
already reveals a distinct pattern regarding the past occur- Titschack et al. 2016). These values are in the upper range of
rence of L. pertusa and M. oculata. aggradation rates obtained so far for other coral mound areas
During the last glacial period, a reduced occurrence of in the North Atlantic (see compilation by Wienberg and
both species in the AS is assumed as only two glacial ages Titschack 2017), and preliminary results of mound records
have been obtained so far (see Dubois-Dauphin et al. 2016), of the West Melilla province and the East Cabliers bank seem
which comprise just 2% of all available ages. However, the to display a very similar pattern (Lo Iacono et al. 2016; Wang
low number of glacial coral ages could also be ascribed to et al. 2016). During the late Younger Dryas and the mid- to
the lack of appropriate core material covering longer Late Holocene, mound aggradation rates decreased
timescales. Yet, preliminary dating results obtained from noticeably to values of ~30–50 cm kyr−1 and < 20 cm kyr−1,
70-m-long drill cores collected from the East Melilla respectively. Thus, although CWC still colonised the East
province (Hebbeln et al. 2015) revealed that there was indeed Melilla mounds during these time intervals, mound
no sustained occurrence of L. pertusa and M. oculata lasting aggradation slowed-down or even stagnated. This reduction
since ~100,000 years BP until the last deglaciation, thus a in mound aggradation can be explained by the environmental
time span covering the last glacial, and part of the preceding change to less favourable conditions for the corals themselves,
interglacial (Krengel et al. 2015). There is a conspicuous but might also be the consequence of a reduced sediment
common start-up phase for their occurrence coinciding with supply.
the onset of the Bølling-Allerød (BA) warm interval at A third species-related pattern comes up when consider-
~14,600 years BP (Fig. 7.1b), which marked the onset of the ing ages obtained for L. pertusa and M. oculata separately
last deglaciation with a post-glacially rising sea level (Fink (Fig. 7.1c). Periods of pronounced CWC occurrence
et al. 2013; Stalder et al. 2015; Lo Iacono et al. 2016; see associated with high coral mound aggradation rates during
Vertino et al., this volume and references therein). The first the last deglaciation and the Early Holocene relate to ages
post-glacial period of pronounced coral occurrence lasted obtained for L. pertusa, while M. oculata seems to have been
until the mid-Younger Dryas (~12,200 years BP) and is largely absent from the AS before the onset of the Holocene.
followed by a second boost roughly covering the entire Early On the contrary, since the mid-Holocene, M. oculata seems
Holocene (11,600–8,300 years BP; Fig. 7.1b). Both periods to dominate over L. pertusa (Fig. 7.1c). A similar pattern is
of pronounced coral occurrence coincided with intensified also shown by faunal analyses based on mound records,
intermediate water mass circulation and enhanced which revealed that M. oculata becomes more abundant
productivity in the surface ocean increasing the availability since the Early Holocene eventually culminating in a M.
of food for CWC (Cacho et al. 2002; Fink et al. 2013, 2015; oculata-dominated coral community (Stalder et al. 2015; Lo
60 C. Wienberg
Iacono et al. 2016). Moreover, as the dominance of M. ocu- the 1st international carbonate mound conference, Monte Veritá,
1–5 November 2015
lata coincides with periods of low mound aggradation rates Lo Iacono C, Gràcia E, Diez S, et al (2008) Seafloor characterization
(Fig. 7.1c), it can be speculated that this species is not as and backscatter variability of the Almería Margin (Alboran Sea, SW
successful and efficient in building-up mounds as L. pertusa. Mediterranean) based on high-resolution acoustic data. Mar Geol
This might be explained by the thinly branching framework 250:1–18
Lo Iacono C, Gràcia E, Ranero CR, et al (2014) The West Melilla cold
formed by M. oculata which does not allow a sufficient baf- water coral mounds, eastern Alboran Sea: morphological character-
fling of sediment and therefore might inhibit enhanced verti- ization and environmental context. Deep-Sea Res Part 2 Top Stud
cal mound aggradation. Oceanogr 99:316–326
It is still not known which environmental change trig- Lo Iacono C, Huvenne VAI, Gonzalez LV, et al (2016) Living reefs
and CWC mounds in the Alboran Sea (Western Mediterranean).
gered the obvious shift in coral species dominance during the Holocene evolution and present-day conditions. In: Abstracts of
Holocene in the AS. It might be the consequence of the the 6th international symposium on deep-sea corals, Boston, 11–16
increasing bottom water temperatures to which M. oculata is September 2016
likely to be more tolerant, as it occurs preferentially in Margreth S, Gennari G, Rüggeberg A, et al (2011) Growth and demise
of cold-water coral ecosystems on mud volcanoes in the west
warmer waters (8.5–10 °C), while L. pertusa seems to domi- Alboran Sea: the messages from the planktonic and benthic fora-
nate in colder waters (6.5–8 °C; Wienberg and Titschack minifera. Mar Geol 282:26–39
2017). This assumption is further supported by experimental Muñoz A, Ballesteros M, Montoya I, et al (2008) Alborán Basin, south-
studies showing that both species have their specific thermal ern Spain. Part I: Geomorphology. Mar Petrol Geol 25:59–73
Naumann MS, Orejas C, Ferrier-Pagès C (2014) Species-specific phys-
preferences and tolerances, with M. oculata showing accli- iological response by the cold-water corals Lophelia pertusa and
matisation capacity toward the presumed CWC upper ther- Madrepora oculata to variations within their natural temperature
mal tolerance limit of 14 °C (Naumann et al. 2014). Overall, range. Deep-Sea Res Part 2 Top Stud Oceanogr 99:36–41
this highlights that a detailed knowledge of bio-ecological Palomino D, Alonso B, Lo Iacono C, et al (2015) Seamounts and
Seamount-like structures of the Alborán Sea. In: Würtz M, Rovere
dynamics of the CWC species adopted for stratigraphic stud- M (eds) Atlas of the Mediterranean seamounts and seamount-like
ies is of utmost importance when interpreting coral age data- structures. IUCN, Gland, Málaga, pp 21–58
sets in a regional, climatological and palaeoceanographic Palomino D, Vázquez J-T, Ercilla G, et al (2011) Interaction between
context (see also Vertino et al., this volume). seabed morphology and water masses around the seamounts on the
Motril marginal plateau (Alboran Sea, western Mediterranean).
Geo-Mar Lett 31:465–479
Acknowledgements This study contributes to the project of the Stalder C, Vertino A, Rosso A, et al (2015) Microfossils, a key to unravel
Deutsche Forschungsgemeinschaft (DFG) “MoccAMeBo” (grant HE cold-water carbonate mound evolution through time: evidence from
3412/18). Jürgen Titschack is acknowledged for compiling the map of the eastern Alboran Sea. PLoS One 10:e0140223
the Alborán Sea. Claudio Lo Iacono and Paolo Montagna are thanked Titschack J, Fink HG, Baum D, et al (2016) Mediterranean cold-
for their very helpful comments on an earlier version of this manuscript. water corals – an important regional carbonate factory? Depos Rec
And finally, all colleagues contributing to the steadily increasing num- 2:74–96
ber of coral ages are thanked for their tremendous efforts. Wang H, Wienberg C, Titschack J, et al (2016) Past cold-water coral
growth in the West Melilla cold-water Coral Province, Alboran Sea,
related to high food availability. Rapp Comm Int Mer Médit 41:58
Wienberg C, Titschack J (2017) Framework-forming scleractin-
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Drop Chapter
Highly Variable Submarine Landscapes 8
in the Alborán Sea Created
by Cold-Water Corals
Dierk Hebbeln
Abstract
in comparison to the surrounding seabed (Wienberg and
Impressive seafloor structures formed by cold-water cor- Titschack 2017). Combined with the high carbonate produc-
als characterise parts of the seafloor in the southeastern tion of CWC and accompanying species this results within
Alborán Sea, forming the East Melilla Cold-Water Coral millennia in the creation of sometimes impressive mound
Mound Province. These geomorphological features are structures, affecting the large-scale heterogeneity of the sea-
composed of a mixture of cold-water coral fragments and floor (Lo Iacono et al. 2018). The development of these coral
hemipelagic sediments, displaying typical coral mound mounds, which largely consist of fossil CWC assemblages
deposits. Along a N-S transect across the Mediterranean embedded in hemipelagic sediments (Dorschel et al. 2005;
Moroccan margin, extending for up to ~25 km, three belts Titschack et al. 2016), is very sensitive to climatic variations.
of very differently shaped mound structures occur. Their As the delivery of food particles to feed the sessile CWC and
morphologies and dimensions vary considerably, ranging sediments to fill and stabilise the biogenic framework con-
from up to 20-km-long and 150-m-high steep ridges to struction are prerequisites for mound formation, the occur-
elongated and arcuate mounds of a few hundred meters in rence of these structures usually is linked to rather strong and
diameter and up to 40 m in height. Obviously, different turbulent hydrodynamics (Mienis et al. 2014; Hebbeln and
interacting drivers, including tectonics and hydrodynam- Samankassou 2015; Wienberg and Titschack 2017).
ics, must have been involved at a variable scale in shaping Consequently, geologic records show that CWC mounds
these fascinating submarine landscapes in the past. typically co-occur with contouritic deposits (Hebbeln et al.
2016; Rebesco and Taviani, this volume).
Keywords Although CWC have been found all over the Atlantic
Cold-water coral mounds · Alborán Sea · Multibeam basin from the shelf down to the mid-Atlantic ridge
echosounder bathymetry · Mound shape · Tectonics · (Mortensen et al. 2008), coral mounds, due to their depen-
Hydrodynamics dency on sediment supply (e.g., Hebbeln et al. 2016), are
restricted to the continental margins of the Atlantic Ocean
and occur from Ireland (Kenyon et al. 2003) southward to
Argentina (Muñoz et al. 2012). They range in height from
Over millennia and longer time scales, framework-forming just a few meters to >300 m (Mienis et al. 2006), and are
cold-water corals (CWC) are able to trigger the development found sometimes as isolated features or mostly grouped in
of large geo-bioconstructions known as coral mounds large clusters or provinces covering hundreds to even thou-
(Roberts et al. 2006; Wienberg and Titschack 2017). As sands of square kilometers (e.g., de Mol et al. 2002, Hebbeln
ecosystem engineers, CWC are key organisms to form highly et al. 2014, Vandorpe et al. 2017). Due to the high accumula-
diverse ecosystems in the deep sea, providing a habitat for tion rates, mound deposits potentially provide very high-
many other marine organisms (Roberts et al. 2006). Given resolution paleoarchives and might even preserve
the availability of suspended sediments, the baffling effect of stratigraphic records that are lacking in the neighboring sedi-
CWC frameworks favors an enhanced sediment deposition mentary succession (Hebbeln et al. 2016). These paleoar-
chives document the development of the CWC ecosystem
D. Hebbeln (*) through time as well as any related changes of the ambient
MARUM – Center for Marine Environmental Sciences, University environmental setting – both of which can be reconstructed
of Bremen, Bremen, Germany through paleoceanographic approaches (e.g., Dorschel et al.

https://doi.org/10.1007/978-3-319-91608-8_8
62 D. Hebbeln
2005; Kano et al. 2007; Wienberg et al. 2018; Montagna and floor (Fig. 8.1d), (iii) finally, the southernmost belt comprises
Taviani, this volume). sinuous to elongated coral ridges, stretching on average in a
Whereas CWC communities are widespread in the NW-SE direction and being partly buried (Fig. 8.1e).
Mediterranean Sea (Freiwald et al. 2009; Chimienti et al., Each mound and ridge structure that was sampled by
this volume), only few coral mound sites have been described gravity and/or box corers (n > 13), is clearly identified as a
up to now. Such coral mounds with heights generally <25 m coral mound/ridge through the composition of its deposits
occur (i) in the Ionian Sea off Santa Maria de Leuca (Taviani comprising CWC fragments and hemipelagic sediments
et al. 2005; Savini and Corselli 2010), (ii) south off Pantelleria (Fig. 8.2; Hebbeln et al. 2009, 2015; Fink et al. 2013; Stalder
Island in the Sicily Channel (Martorelli et al. 2011), (iii) in et al. 2015). At four sites (Brittlestar Ridges I and III, Mole
the Tyrrhenian Sea (Remia and Taviani 2005), and (iv) in the and Dragon Mounds; see Fig. 8.1b), drill cores obtained with
northern Alborán Sea, from where several small mound the Bremen seafloor drill rig MeBo confirmed the CWC
structures have been reported (Muñoz et al. 2008; Lo Iacono mound nature of these structures even down to drill depths of
et al. 2008, this volume), although evidence for their true 33–70 m (Hebbeln et al. 2015). Consequently, it is assumed
nature (formed by CWC, bryozoans or others) is partly still that the totality of the mound and ridge structures identified
lacking. in the EMCP are build-up by CWC.
The most impressive coral mound province of the The three Brittlestar Ridges in the north are very long and
Mediterranean Sea has been described from the southern steep coral ridges, rising 50–150 m above the surrounding
Alborán Sea. Framed in the west by the West Melilla CWC sea floor between 475 and 375 m and stretching from over
Province (WMCP) with mounds reaching heights of up to 3 km to almost 20 km in length (Fig. 8.1b, c). Interestingly,
50 m (Lo Iacono et al. 2014) and in the northeast by the although they are all attached to the southern edge of the
Cabliers Mounds (Lo Iacono et al. 2018), the East Melilla Banc de Provençaux, they extend into very different
CWC Province (EMCP, Fig. 1) comprises coral mounds directions (Brittlestar Ridge (BR) I: beginning southward
displaying an impressive variety of shapes and sizes, partly and turning southeastward, BR II: southwestward, BR III:
reaching heights of >100 m. Located off the Moroccan coast beginning southwestward and turning WNW-ward). The
east off the Spanish enclave Melilla, the EMCP was first elongated shape of coral mounds is often controlled by a
mentioned by Comas and Pinheiro (2007) and described in dominant unidirectional bottom current (e.g., Messing et al.
more detail by Fink et al. (2013). 1990; Correa et al. 2012; Hebbeln et al. 2014), which due to
While in the WMCP no living corals have been observed, the varying directions of the Brittlestar ridges appears rather
scattered occurrences of the two most common CWC, unlikely here. Nevertheless, although probably not
Lophelia pertusa and Madrepora oculata, have been reported controlling the shape of the ridges, strong bottom currents
from the EMCP (Hebbeln et al. 2009; Fink et al. 2013). Very clearly had a role in their development, as demonstrated by
high mound aggradation rates of several meters per thousand the distinct moats found at the base of the ridges. Moats are
years during the last deglaciation and the Early Holocene most pronounced and deep around Brittlestar Ridge I, which
clearly document much more favorable living conditions for point to a stronger bottom current impact to this easternmost
the CWC in the EMCP during the past (Fink et al. 2013; ridge – at least for the most recent development that is best
Wienberg, this volume). reflected in the present-day seabed morphology.
Here, a high resolution bathymetric map of the EMCP is Peculiar features of the western Brittlestar Ridge III are
presented to document a large variety of submarine the abrupt changes in direction of partly almost 90° that are
landscapes triggered and maintained within millennia by occasionally observed along its crest (Fig. 8.1b). This
CWC growth (Fig. 8.1). The bathymetric dataset consists of configuration might hint to a tectonic control of the
multibeam echosounder data obtained with a KONGSBERG orientation and extension of the ridges, especially as the
EM1002 operating at 95 kHz during the MSM36 cruise in dominant directions to the SE and the SW follow the main
2014, aboard the RV Maria S. Merian (Hebbeln et al. 2015). regional fault directions (Ammar et al. 2007; Martínez-
It shows a huge variability of remarkable seabed features, García et al. 2011). However, the drill cores obtained from
which are arranged in three east-west-trending belts between the Brittlestar Ridges I and III confirm their CWC mound
the shallow Banc de Provençaux to the north (a volcanic nature down to maximum drill depths of 70 m and 30 m,
structure of Miocene age; Ammar et al. 2007), and the respectively (Hebbeln et al. 2015), indicating that tectonics
Moroccan coast to the south (Fig. 8.1b). (i) In the northern probably only played a role of a pre-conditioning factor for
sector of this region, the three so-called Brittlestar Ridges mounds to initiate, by providing a hardground for the first
(Hebbeln et al. 2009; Fink et al. 2013) are attached to the CWC communities to settle.
southern edge of the Banc de Provençaux (Fig. 8.1c), (ii) Separated by a seabed area barren of any mound struc-
southward, a cluster of at least 25 coral mounds with oval to tures, a cluster with oval- to arcuate-shaped mounds occurs
arcuate shape occurs on an area with a gently rising flat sea to the south of the Brittlestar Ridges, in water depths of 230–
8 Submarine Landscapes in the Alborán Sea and Cold-Water Corals 63
Fig. 8.1 The East Melilla Cold-Water Coral Mound Province (EMCP): indicate the position of the detailed maps in (c) (d) and (e); (BR
(a) Overview map showing the location of the EMCP in the Alborán Brittlestar Ridge, MM Mole Mound, DM Dragon Mound). (c) to (e)
Sea. (b) Multibeam bathymetric map of the EMCP (25 m grid resolu- Detailed multibeam bathymetric maps (10 m grid resolution; approx.
tion) showing the three main morphotypes of coral ridges/mounds 4.5 km wide) showing each of the main coral ridge/mound type (for
which are arranged along east-west trending belts. White rectangles location see (a))
320 m (Fig. 8.1b, d). These mounds are much smaller coming to extended, almost ridge-like, structures towards
pared to the Brittlestar ridges as their longest axes just reach WSW, where they get closest to the ridges of the southern-
few hundreds of meters. These mounds display very steep most zone (Fig. 8.1b). The intermediate shape of these
flanks, often reaching slope angles of >30°. Average heights slightly elongated mounds – between oval- and ridge-like
above the seafloor range between 20 and 40 m, and even mounds – occurs where both morphotypes come closest to
more if the depressions of the surrounding moats are con- each other, pointing to an environmental control on the
sidered. The extensions of these moats (Fig. 8.1d) point to mound shapes.
bottom currents predominantly moving along northwest- In the southernmost part of the EMCP, coral ridges
southeast directions, however, without any clear indication arranged in an E-W trending belt in water depths of 200–
to either NW- or SE-directed bottom currents. 240 m rise to only ~10 m above the surrounding sea floor
These oval/arcuate mounds are distributed across an (Fig. 8.1b, e). Vanishing towards the south, these ridges
ENE-WSW direction, with their shapes gradually chang- appear to get buried by a thin veneer of sediments. The
64 D. Hebbeln
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312:543–547 geography of Mediterranean cold-water corals
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Alborán Sea: from coral mounds and species dominance
Spatio-Temporal Distribution
of Mediterranean Cold-Water Corals 9
Agostina Vertino, Marco Taviani, and Cesare Corselli
Abstract boundary. “Golden ages” for the species Lophelia pertusa,

Cold-water corals have inhabited the Mediterranean basin and large bioconstructions formed by this coral, are thus far
since at least the Miocene, undergoing important modifica- known in the Early Pleistocene (Calabrian stage), at the
tions through time. Most information regarding pre-Pleisto- boundary Bølling- Allerød – Younger Dryas and in the Early
cene occurrences of extant cold-water coral species still Holocene (at least in the western basin). A large knowledge
relies on ancient literature records in need to be updated gap currently exists between the end of the Calabrian stage
according to modern taxonomic and chronostratigraphic and the last 50 kyr BP. Several Atlantic deep-sea species
concepts. In this chapter, Neogene and Quaternary coral (including frame-building and “psychrosperic” cold-water
records are discussed. Many occurrences have been revised corals), common in the Early Pleistocene, disappeared in
from the taxonomic point of view through the analysis of the Mediterranean after the Late Pleistocene, but how and
historical museum collections, newly collected specimens when this event occurred is not known yet. Further studies
and original species descriptions and illustrations. In particu- need to be carried out to understand if there is any correla-
lar, this study summarises the current state of knowledge on tion between this deep-sea basin-scale extinction and the
Mediterranean frame-building cold-water corals and associ- decline of Lophelia-dominated bioconstructions observed
ated solitary species from the Miocene onwards. Several in the late Younger-Dryas and after the Early Holocene. In
growth and demise phases, as well as changes in composi- order to fill knowledge gaps on the fossil record of
tion of dominant species have been observed so far. A shift Mediterranean cold-water corals and to fully exploit the
from Dendrophyllia- to “Atlantic-like” Lophelia-dominated valuable potential of these organisms as palaeoenvironmen-
paleocommunities occurred at the Pliocene – Pleistocene tal archives, the setup of a comprehensive open access data-
base, including quality-controlled data on both modern and
fossil species, is highly recommended. This would also pro-
Electronic supplementary material The online version of this chapter
(https://doi.org/10.1007/978-3-319-91608-8_9) contains supplemen-
vide a useful tool for managing, valorising and preserving
tary material, which is available to authorized users. the unique, yet undervalued paleontological heritage of the
Mediterranean regions.
A. Vertino (*)
Department of Earth and Environmental Sciences, Milano-Bicocca Keywords
University, Milan, Italy
Cold-water coral · Mediterranean · Neogene · Quaternary
Department of Geology, Renard Centre of Marine Geology, Ghent · Deep-sea · Bioconstruction
University, Ghent, Belgium
M. Taviani
9.1 Introduction
Woods Hole, MA, USA
The mineralised skeleton of cold-water corals (CWC), such
as Scleractinia, Coralliidae, Isididae and Stylasteridae, is
C. Corselli suitably preserved in the fossil record providing important
Department of Earth and Environmental Sciences, Milano-Bicocca information on ancient deep-sea paleoenvironments (e.g.,
University, Milan, Italy Vertino 2003; Roberts et al. 2009; Robinson et al. 2014;

https://doi.org/10.1007/978-3-319-91608-8_9
68 A. Vertino et al.
Taviani et al., this volume; Montagna and Taviani, this vol- ciated solitary ones in the peri-Mediterranean region through
ume; Angeletti et al., this volume). A crucial role in this the Neogene and Quaternary. These coral records are
regard is played by frame-building scleractinian species, like reported on a georeferenced map and most of them are taxo-
Lophelia pertusa and Madrepora oculata. These species nomically revised based upon the analysis of historical
construct considerable carbonate structures, hosting a variety museum collections, newly collected specimens and original
of associated mineralised macro- and microorganisms, only species descriptions and illustrations. This is the first step
in certain environmental conditions (Freiwald et al. 2004; towards setting a much needed database of fossil and recent
Roberts et al. 2009; Henry and Roberts 2016; Wienberg and CWC in the Mediterranean basin.
Titschack 2017; Rueda et al., this volume; Weinbauer et al.,
this volume).
The genera Lophelia and Madrepora boast a significant 9.2 Material and Methods
geological antiquity, with representatives being known since
the Mesozoic (Cretaceous) (Madrepora: Stolarski and The spatio-temporal data presented herein derive from the
Vertino 2007) and Cainozoic (Miocene) (Lophelia: Roberts critical analysis of modern and ancient published literature
et al. 2009 and references therein), respectively. At present (Appendices 9.1, 9.2 and 9.3; Fig. 9.3) and direct observations
Lophelia pertusa and Madrepora oculata play a pivotal role of Miocene to Holocene Mediterranean coral specimens
in engineering CWC bioconstructions in the Atlantic and (Figs. 9.1 and 9.2). This study focuses on the most common
Mediterranean (e.g., Freiwald et al. 2004; Taviani et al. extant frame-building CWC taxa (Fig. 9.1) (Lophelia
2005b; Roberts et al. 2009; Corselli 2010; see Altuna and pertusa, Madrepora oculata, Enallopsammia scillae, the
Poliseno, this volume; Chimienti et al., this volume) although genus Dendrophyllia, with morphotypes resembling modern
the two species display a wider geographical distributional deep-sea species) and associated solitary scleractinians
range (see Roberts et al. 2009). They are generally associated (Fig. 9.2) (Desmophyllum dianthus, Caryophyllia coronata,
with other habitat-forming corals of lower frame-building Caryophyllia calveri, Stenocyathus vermiformis and the
potential, like the solitary gregarious Desmophyllum dian- genus Javania) that have characterised Mediterranean deep-
thus, the colonial Dendrophyllia cornigera and, restricted to sea bioconstructions during the Quaternary and whose
the NE Atlantic, Dendrophyllia alternata, Eguchipsammia occurrence is known since the Miocene. Museum collections
cornucopia, and Enallopsammia scillae (= rostrata = amphe- of Miocene to Early Pleistocene fossil corals, critically
lioides) (Zibrowius 1980; Roberts et al. 2009 and references examined in this study for their CWC material, are listed in
therein). Additionally, solitary scleractinian species, such as Vertino et al. (2014) and updated in the acknowledgements
Caryophyllia aradasiana (= calveri) and Stenocyathus ver- section of the present chapter. Additional analyses were
miformis in the Mediterranean, and Caryophyllia coronata performed on submerged Quaternary specimens held in the
(= sarsiae) in the NE Atlantic, are typical components of Department of Environmental and Earth Sciences, University
Lophelia-Madrepora bioconstructions (e.g., Zibrowius of Milano-Bicocca (Italy) and the Institute of Marine
1980; Freiwald et al. 2009; Mastrototaro et al. 2010; Angeletti Sciences – CNR, Bologna (Italy).
et al. 2014; Taviani et al. 2017; Vertino et al. 2015; Altuna The on-land CWC occurrences reported in Fig. 9.3 and
and Poliseno, this volume; Chimienti et al., this volume; Appendix 9.1 are not comprehensive: they include only the
Rueda et al., this volume). Most of these species are known scleractinian species mentioned above and exclusively lit-
in the Quaternary (Vertino 2003; Taviani et al. 2011) and, erature citations taxonomically reviewed in recent years.
some of them, in the Neogene record of the Mediterranean The accuracy of the geographic location of the analysed on-
(Taviani et al. 2005a; Vertino et al. 2014). However, the exact land sites is highly variable. In some cases only a generic
geographic location and precise age of fossil CWC occur- geographic description was given in old publications, there-
rences on-land is lacunose in many cases, and taxonomic fore exact geographic coordinates are not always available.
identification often dubious since many records refer to old The radiometric coral ages reported in Figs. 9.4 and 9.5
literature accounts. Data regarding the spatio-temporal dis- (Appendices 9.2 and 9.3) derive from the literature: Hersey
tribution of submerged Late Quaternary CWC in the (1965), Zibrowius (1980, 1981), Taviani and Colantoni
Mediterranean Sea are still limited but much more accurate (1984), Delibrias and Taviani (1985), Schröder-Ritzrau
because based on samples obtained using recent advanced et al. (2005), Malinverno et al. (2010), McCulloch et al.
positioning systems. Moreover, thanks to the general good (2010), Angeletti and Taviani (2011), Frank et al. (2011),
preservation of Late Pleistocene and Holocene corals, it is Taviani et al. (2011), Fink et al. (2012, 2013, 2015), Stalder
possible to directly date coral skeletons using radiometric et al. (2015), Titschack et al. (2016), and Dubois-Dauphin
techniques (e.g., McCulloch et al. 2010; Fink et al. 2015; et al. (2016, 2017). In order to compare radiocarbon ages,
Wienberg and Titschack 2017). 14
C data not included in Fink et al. (2015), were re-calibrated
This chapter aims at providing an updated overview of the by using the Marine13 calibration curve (Reimer et al. 2013)
known occurrences of constructional CWC species and asso- of the Oxcal 4.3.2 software (Bronks Ramsey 2009) assum-
Fig. 9.1 Miocene to Holocene examples of Mediterranean frame- pertusa (Early Pleistocene, “La Montagna”, Messina, southern
building cold-water corals (CWC). (a and b) Dendrophyllia cf. cor- Italy), scale bar 2 cm. (e) Fossil coral rubble dominated by tiny
nigera (Miocee, Serravallian-Upper Tortonian, surroundings of branches of Madrepora oculata (Early Pleistocene, San Filippo,
Lecce, southern Italy); see Vescogni et al. 2018; (a) Fossil coral Messina, southern Italy), scale bar 1 cm. (f) Fresh-looking to dark-
rubble, scale bar 2 cm; (b) Transversal section of a juvenile corallite, coated fragments of Madrepora oculata on the surface of a box-core
scale bar 0.5 cm. (c) Enallopsammia scillae (Early Pleistocene, “La samples (MD194 cruise, BC 3471) collected at 314 m depth in the
Montagna”, Messina, southern Italy), scale bar 1 cm. (d) Lophelia Alboran Sea (Holocene), scale bar 2 cm
Fig. 9.2 Miocene to Late Pleistocene examples of Mediterranean soli- Capo Milazzo, southern Italy), scale bar 1 cm. (c) Distal view of a well
tary corals associated with frame-building CWC. (a and b) Lateral (a) preserved corallite of Stenocyathus vermiformis (Early Pleistocene,
and distal (b) view of large specimens of the gregarious species Gravitelli, Messina, southern Italy), scale bar 2 mm; (d) Black coated
Desmophyllum dianthus, embedded in coral rudstones (a: Early specimen of Caryophyllia coronata collected off-shore Crete at 2133 m
Pleistocene, Trapani, Messina, southern Italy; b: Early Pleistocene, depth (GECO cruise, 50) (Late Pleistocene), scale bar 1 cm
ing a reservoir effect of ~400 years (Siani et al. 2001), and Zibrowius, 1980, Caryophyllia calveri Duncan, 1873 and
are reported as Median Probability Age (MPA) (Appendix Enallopsammia rostrata (Pourtalès, 1878) that, according to
9.2). This procedure has been followed also for data pub- Vertino (2003) and following the Principle of Priority of the
lished over 30 years ago by Hersey (1965), Zibrowius International Code of Zoological Nomenclature (ICZN)
(1980), (1981), and Taviani and Colantoni (1984). However, [Art. 23.1], are named herein as Caryophyllia coronata
due to the little methodological information provided by Seguenza, 1864, Caryophyllia aradasiana Seguenza, 1864
these authors on the obtained 14C data, the related calibrated and Enallopsammia scillae (Seguenza, 1864), respectively.
ages (indicated with an asterisk in Fig. 9.4 and Appendix Based on comprehensive molecular and morphological anal-
9.2) must be taken with caution. yses, Addamo et al. (2015a), Addamo (this volume) high-
Scleractinian taxonomy follows WoRMS Editorial Board lighted the extreme similarity between the scleractinian
(2017), with the exception of Caryophyllia sarsiae species D. dianthus and L. pertusa (99.8% of mitochondrial
9 Spatio-Temporal Distribution of Mediterranean Cold-Water Corals 71
Fig. 9.3 (a) Overview map showing the spatio-temporal distribution of grained siliciclastic deposits or mud-dominated sediment and boulders;
the on-land and submerged CWC sites mentioned in the text and/or corals encrusting subvertical walls and overhangs; coral frameworks
listed in Appendices 9.1, 9.2 and 9.3. (b and c) Detail of southern Italy forming bioconstructions. Map source ESRI. Numbers refer to the
(b) and northern Italy (c) including basic information on the most com- CWC sites listed in Appendix 9.1
mon (paleo)habitats: coral colonies and/or fragments sparse in fine-
nucleotides and 97% of microsatellite sequence are identi- research on modern specimens and pending taxonomic revi-
cal). This finding strongly suggests that, despite their differ- sion of fossil species historically assigned to these genera.
ent growth forms (solitary vs. colonial), these two species The terms zooxanthellate, azooxanthellate, constructional
should be ascribed to a single genus and, following the ICZN (= frame-building) and non-constructional are used in the
Principle of Priority, L. pertusa should be named as text following the definition by Schumacher and Zibrowius
Desmophyllum pertusum. Nevertheless, in this chapter we (1985) and the words circalittoral and bathyal are adopted sensu
maintain the traditional division due to ongoing genetic Pérès and Picard (1964) (see Altuna and Poliseno, this volume).
Fig. 9.4 Distribution of radiometric ages of Late Pleistocene and of coral specimens (dated through 14C or U-Th) whose age is included
Holocene Mediterranean coral specimens collected from submerged in those 500 years. Cs Caryophyllia sarsiae (=coronata), Cc
cold-water coral sites of the Mediterranean Sea. Coral compilation Caryophyllia calveri, Dd Desmophyllum dianthus, Lp Lophelia per-
from the literature; see references in the text and complete age list in tusa, Mo Madrepora oculata. Asterisks indicate 14C coral ages
Appendices 9.2 and 9.3. The width of each black bar corresponds to published in the 1980s that must be treated with caution
500 years. The height of each black bar corresponds to the number (N)
Fig. 9.5 Ages of L. pertusa (Lp) and M. oculata (Mo) collected from The height of each black bar corresponds to the number of coral speci-
the Melilla coral mounds (a) and the Santa Maria di Leuca mounds (b) mens (dated through 14C and/or U-Th) whose age is included in those
in the last 16 kyr. The width of each black bar corresponds to 500 years. 500 years
These adjectives are applied to fossil species, and/or assem- and advanced techniques, such as the use of geochemical
blages, based on the actualistic assumption that the ecologi- proxies, when possible.
cal requirements of extant taxa have not drastically changed
through geological time. Finally, the adjective deep is used in 9.3.1.1 Miocene
this chapter to indicate low circalittoral to bathyal (paleo) One of the richest regions in terms of specimens and species
environments. abundance of Miocene corals is located in northern Italy. In
particular, the diversified coral assemblages of the “Collina
di Torino” (TH = Turin Hills) deposits have been the focus of
9.3 Cold-Water Corals Through Geological taxonomic and paleoecological studies carried out in the
Times eighteenth century by Sismonda (1871) and De Angelis
(1894) and later by Zuffardi-Comerci (1932) and Chevalier
9.3.1 Key Study Sites (1961). Some of the “Helvetian” fossil coral localities men-
tioned by Chevalier (1961) (Valle Ceppi, Val Sanfrà, Monte
Fossil occurrences of CWC are known since the Miocene in Cappuccini) have been recently assigned to the Burdigalian
several peri-Mediterranean localities. Among the examined “Termofourà Formation” and the Langhian “Baldissero
sites (Appendices 9.1, 9.2 and 9.3; Fig. 9.3), there are some Formation” (Zunino and Pavia 2009). The richest fossilifer-
exceptional ones in terms of outcrop extension and exposure ous layers of the TH formations correspond to conglomerate
and/or preservation and diversity of the fossil assemblages. lenses interbedded with silt-clay deposits, described by
They are shortly described in the following paragraphs and Chevalier (1961) as a “mélange” of “hermatypic and aher-
suggested as target sites for more detailed taxonomic, strati- matypic forms”. Based upon taxonomic and taphonomic
graphic and paleoecological analyses combining traditional arguments on mollusc assemblages in the Termofourà and
Baldissero Formations, it has been hypothesised that the
shallow-water components were transported down basin M. oculata (cited in the literature as Amphihelia), E. cf. scil-
through gravity processes in submarine canyons, and got lae and D. dianthus have been cited in at least one of the
mixed with deeper water faunal elements (Zunino and Pavia Tortonian localities of northern Italy (Appendix 9.1).
2009 and references therein). Through the ongoing revision Of particular interest are the coral assemblages of the
of the historical coral collection held at the Museum of Tortonian “Calcare di Mendicino” (CM), located at Belsito,
Natural History of the Torino University and of newly colin Calabria (southern Italy), where bioconstructed CWC
lected specimens from the “Valle Ceppi” and “Val Vergnana” limestones up to 3 m in thickness occur (Mastandrea et al.
localites, we have ascertained that the TH deposits contain 2002). Through thin section analysis Mastandrea et al.
several CWC specimens, most of which represented by soli- (2002) identified the dominant corals as Dendrophyllia and
tary corals typical of muddy to fine sandy deposits. Among Oculina and clearly showed the common presence of associ-
frame-building CWC, the genus Dendrophyllia is rather ated stylasterid specimens. Due to the almost complete ara-
common and some fragments show size and shape compa- gonite dissolution, scleractinians were not identified at
rable to that of the modern species D. cornigera. Other den- species level. However, further detailed analyses of the coral
drophylliids, identified as Enallopsammia scillae in the inner and outer moulds may provide important additional
historical collections, belong indeed to the genus taxonomic details. The only other known occurrence of
Enallopsammia but are indicated herein as Enallopsammia Miocene CWC rudstones is located in the surrounding of
cf. scillae due to the larger size of their corallites with respect Leuca, Apulia (southern Italy), where a very dense accumu-
to the Pleistocene Mediterranean and modern Atlantic spe- lation of dendrophylliid (including Dendrophyllia cf. corni-
cies. Several specimens originally named as “Amphihelia” gera, Fig. 9.1a, b) and caryophylliid corals form a much
and “Diplohelia” (Zuffardi-Comerci 1932; Chevalier 1961) thinner layer, up to 25 cm in thickness, corresponding to the
can be ascribed to the modern species M. oculata (Fig. 14.4h condensed lower Serravallian-upper Tortonian phosphate-
in Vertino et al. 2014). Moreover, the skeletal features of rich deposit known in the literature as “Aturia Layer” (Föllmi
most coralla of Desmophyllum, ascribed by Chevalier (1961) et al. 2015; Vescogni et al. 2018). Finally, dendrophyliids
to 16 distinct species, fall within the high intraspecific vari- branches (likely Dendrophyllia spp.) occur embedded in
ability of the modern species D. dianthus (Addamo et al. methanogenetic limestones from various sites in the northern
2015b). So far, coral fragments belonging to the species L. Apennines such as the sites Ca’ Fornace in the Sintria Valley,
pertusa and S. vermiformis have not been found in the Ravenna and Montepetra Forlì, in Emilia-Romagna (Kiel
Miocene TH deposits. Javania has been cited in ancient lit- et al. 2018; Taviani unpublished data).
erature but its presence has still to be ascertained. Several Lastly, it is worth citing the exceptionally well preserved,
Caryophyllia specimens have been collected from the Early abundant and diversified CWC fauna of the Messinian
Miocene TH deposits but their identification at species level “brèche rouge” of Carboneras (SE Spain), dated to the
has not been revised yet. Messinian stage (Barrier et al. 1991), whose paleobiological
Northern Italy is also well known for several Upper value has been recognised by several authors (e.g. Taviani
Miocene fossil sites containing well preserved azooxanthel- et al. 2005a; Roberts et al. 2009; Freiwald, this volume).
late corals. The Tortonian deep-sea coral fauna is scarce in Scleractinians, gorgonians (Coralliidae, Isididae,
the TH region but rather common, diversified and exception- Primnoidae) and stylasterids (the most diversified known so
ally well preserved in other locations, such as Tortona, far in the fossil record) were living in a heterogeneous deep
Stazzano, Sant’Agata Fossili, Montebaranzone, Montegibbio seafloor characterised by both hard and soft substrates
(De Angelis 1894; Simonelli 1896; Montanaro 1929; (Barrier et al. 1991). The hard substrate, consisting of frag-
Zuffardi-Comerci 1937; Chevalier 1961; Corselli 2001). mented volcanic rocks, provided a suitable colonisable sur-
These sites are mostly characterised by marly and sandy face for a diverse stylasterid community including at least 14
deposits containing typical soft-bottom dwelling solitary species, 10 of which known in the NE Atlantic and 4 living
corals, belonging to the genera Balanophyllia (Eupsammia), today only in Indo-Pacific regions and the tropical Atlantic
Flabellum, Ceratotrochus, Trochocyathus, Deltocyathus, (Barrier et al. 1991). Also among the scleractinians, two of
Stephanophyllia etc. (Vertino et al. 2014 and references the over ten recognised genera living today in the NE
therein). However, several fragments of colonial, and poten- Atlantic, are known only in the modern bathyal fauna of the
tially frame-building corals are also known from these sites. western Atlantic and in Indo-Pacific regions. Like in other
Most probably these colonial corals used skeletal remains of Miocene sites, the family Dendrophylliidae is rather com-
other organisms as substrate for the settlement of their lar- mon and at least three species of Dendrophyllia collected in
vae. In particular, specimens comparable to D. cornigera are the Carboneras outcrop are ascribable to deep-sea N Atlantic
relatively common in marly deposits of both Piedmont and taxa (Barrier et al. 1991). Fragments of the frame-building
Emilia Romagna sites and skeletal fragments identifiable as genera Madrepora and Desmophyllum also occur but there is
no evidence of bioconstructions. Interestingly, the number of (Monegatti et al. 2001; Cau et al. 2015). Another remark-
CWC species collected from the “brèche rouge” is much able Pliocene CWC site is located in the surroundings of
higher than the species number that could be found by dredg- Marmorito (Piedmont, northern Italy) (Appendix 9.1);
ing modern coral-dominated NE Atlantic bathyal seafloors. where coral rudstones are dominated by D. dianthus and E.
The high CWC diversity observable in the Carboneras scillae. They contain secondarily also Caryophyllia cyathus
deposits may have been possibly amplified by time-averaging and other dendrophylliids. Though corals are preserved only
processes. However, a comparable number of species could as moulds, they can be identified at species level through
be found today in coral-rich deep-sea environments of the macro- and micromorphology analysis of casts. Several
tropical Atlantic and in some Indo-Pacific regions (Barrier taxonomic characters (size, shape, branching typology,
et al. 1991; Cairns 2007). number of septa, imprint of wall microarchitecture) hint
also at the presence of L. pertusa in the Marmorito
9.3.1.2 Pliocene deposits.
Most deep-sea azooxanthellate scleractinian genera known Most Pliocene CWC occurrences from southern Italy and
so far are solitary soft-bottom dwelling forms (De Angelis from the eastern Mediterranean (e.g., Seguenza 1880; De
1893, 1894, 1895; Osasco 1895; Simonelli 1895, 1896; Stefano 1899; Barrier 1984, 1987; Roux et al. 1988; Barrier
Zuffardi-Comerci 1927, 1937; Montanaro 1931; Dieni and et al. 1989; Hanken et al. 1996) have been recently ascribed
Omenetto 1960; Chevalier 1961; Russo 1980) ascribable, or to Early Pleistocene deposits (Vertino et al. 2003; Di
comparable, to modern taxa living in muddy to fine sandy Geronimo et al. 2005; Titschack and Freiwald 2005; Di
seafloors (Vertino et al. 2014). The dominance of these cor- Stefano and Longhitano 2009).
als is probably only apparent, being biased by the over-
whelming abundance of Pliocene marly and clayey bottoms 9.3.1.3 Early-Middle Pleistocene
(e.g. “Argille Azzurre Fm”) with respect to hard bottom sub- The most remarkable CWC outcrops so far known in the
strates. Frame-building CWC species are reported in several peri-Mediterranean region are located in southern Italy
Pliocene localities of northern Italy (De Angelis 1894; and are particularly abundant along the margin of the
Osasco 1895; Simonelli 1895; Montanaro 1929, 1931; Messina Strait (Seguenza 1864, 1880; Di Geronimo 1987;
Chevalier 1961; Corselli 1997; Spadini 2015), and Sardinia Zibrowius 1987; Barrier et al. 1989; Roux et al. 1988; Di
(Chevalier 1962) as well as in the Vaucluse region (France) Geronimo et al. 2005; Vertino 2003; Vertino et al. 2014;
and in Catalonia (Spain) (Chevalier 1961) (Appendix 9.1). Taviani et al., this volume and references therein). These
In all these cases corals have been recorded as fragments deposits emerged due to strong regional uplift since the
within fine-grained siliciclastic deposits. The Pliocene sedi- middle Pleistocene. Their facies heterogeneity seems to be
ments of the Siena Basin (SB) are particularly important for related to a complex paleo-strait physiography character-
the diversity of azooxanthellate corals and the very good ised by several micro-basins that evolved independently
preservation state of most skeletons, some of which are through time (Barrier 1987). In particular, in the surround-
probably still preserved as aragonite. A recent review of the ing of the city of Messina, CWCs occur within two main
fossil Scleractinia contained in the Zanclean-Piacenzian facies groups, (1) Carbonate-dominated Facies (CF) and
deposits of the SB (Spadini 2015) lists 19 scleractinian gen- (2) Siliciclastic-dominated Facies (SF) (Vertino et al.
era living today preferentially, or exclusively, in circalittoral 2013). The CF group is characterised by CWC rudstones
to bathyal environments. In particular, the following frame- laterally evolving into carbonate muddy sands and calcar-
building species are reported: dendrophylliid specimens enites. The rudstones consist almost exclusively of skeletal
comparable to D. cornigera, the species E. scillae and D. fragments of frame-building deep- water scleractinians,
dianthus (indicated as “Desmophyllum sp.”). Additionally, such as L. pertusa, M. oculata, E. scillae and D. dianthus
Spadini (2015) reports the first occurrence in the (Figs. 9.1c–e and 9.2a, b) and have been interpreted as, at
Mediterranean Pliocene of the tiny species S. vermiformis, a least partly, in-place bioconstructions. They include sev-
recurrent taxon associated with Pleistocene to recent “White eral other associated species (e.g. C. coronata, and second-
Coral” communities (Vertino 2003; Freiwald et al. 2009; arily, C. aradasiana, S. vermiformis, Dendrophyllia spp.),
Mastrototaro et al. 2010; Rosso et al. 2010; Taviani et al. all living today in NE Atlantic bathyal environments but
2011, 2017; Angeletti et al. 2014; Altuna and Poliseno, this some of them lacking in the modern Mediterranean
volume; Chimienti et al., this volume). Colonial and solitary (Vertino 2003; Vertino et al. 2014; Vertino and Corselli,
CWC, among which dendrophylliids (including this volume; Altuna and Poliseno, this volume). These bio-
Enallopsammia cf. scillae, Vertino unpublished data) and constructed deposits interfinger with floatstones character-
Caryophylliidae, are mentioned from the Stirone River che- ised by mudstone to packstones matrix and dominated by
moherm in the northern Apennines in the Parma province isidid octocorals and brachiopods and/or bryozoans and
echinoderms. The CF CWC species characterise also the dated so far have resulted to be younger than 14 kyrs
lateral and overlying SF facies that consist mostly of marly (Fig. 9.4). However, these ages have been obtained by
and silty clays and, locally, show evidences of chaotic dating coral specimens collected through dredging, box-
mass deposits. In these siliciclastic-dominated deposits coring, grabbing and gravity coring of the upper few meters
frame-
building coral species are commonly scattered of seafloor sediment (Appendices 9.2 and 9.3).
within the fine-grained sediment whereas soft-bottom spe- The Alborán Sea represents the most spectacular CWC
cies, such as Caryophyllia communis and Flabellum spp., mound region known so far in the Mediterranean Sea,
can be rather common. These deposits are rich in frame- both for the wide extension of the mounds (Fink et al.
building species only in the vicinity of large boulders and/ 2013, 2015; Lo Iacono et al. 2014a, b; Wienberg, this vol-
or paleoescarments whose original surface can be still ume) and for the diversified fossil and modern fauna asso-
encrusted by hard-bottom fauna (coral basal parts, ciated to frame-building coral communities (Lo Iacono
cemented bivalves, serpulids, bryozoans etc.) (Barrier et al. 2014b, 2016; Stalder et al. 2015; Lo Iacono et al.
1987; Vertino 2003; Di Geronimo et al. 2005; Taviani 2016; Wienberg, this volume). The largest coral mounds
et al., this volume and references therein). Early Pleistocene of the Eastern Melilla Coral Province seem to be dated
CWC are known from emerged deposits of other back to the Middle Pleistocene (Krengel et al. 2017), but
Mediterranean regions, but our knowledge on frame- data collected so far from superficial deposits indicate
building species is thus far limited to Italian locations that frame-building CWC (at least L. pertusa) were com-
(e.g., Barrier 1987; Placella 1978, 1980; Di Geronimo mon between ~13.5 and 12.5 and ~11.5 and 10.5 kyr BP
1979; Cantalamessa et al. 1987, 1997; Caldara et al. 1993; (Fig. 9.5a; Appendices 9.2 and 9.3), with an apparent
Di Geronimo et al. 2005), Rhodes (Titschack and Freiwald decline phase between ~12.2 and ~11.6 kyr BP (Wienberg,
2005; Titschack et al. 2008; Titschack, this volume), and this volume). These flourishing coral periods correspond
Karpathos (Moissette et al. 2017) (Fig. 9.3; Appendix 9.1). to the highest aggradation rates observed thus far in the
The age of the CWC-rich deposits, dated so far, from these carbonate mounds of the Melilla Province and have been
three localities has been ascribed to the Calabrian stage correlated to intensified intermediate water mass circula-
(Di Stefano and Longhitano 2009; Titschack and Freiwald tion and enhanced productivity in the Alborán Sea
2005; Moissette et al. 2017). Some outcrops from north- (Wienberg, this volume and reference therein).
eastern Sicily, containing scattered highly bioeroded and The Santa Maria di Leuca (SML) Province is the second
mechanically abraded CWC, are probably younger (Middle widest CWC mound area known in the Mediterranean. It is
Pleistocene, Biozone MNN19f) but their coral content located in the eastern basin, along the upper slope of the
seems to be reworked from older beds. The only other Apulian continental margin, at water depth ranging between
information about Middle Pleistocene CWC known hith- ~400 and 1000 m (Taviani et al. 2005b; Savini and Corselli
erto in the Mediterranean derives from research in prog- 2010; Savini et al. 2014; Chimienti et al., this volume).
ress on submerged coral mounds of the Alborán Sea, Recent studies highlighted the presence of 5820 mound-
drilled using the Bremen Seafloor Drill Rig (MeBo) like morphologies over a total area of approximately
(Hebbeln et al. 2015; Krengel et al. 2017; Wienberg, this 600 km2, potentially colonised by CWC (dead or alive)
volume). In this area large seabed structures made up by (Savini et al. 2014). Less than 40% radiometric ages of
CWC occur from 230 to 450 m water depth (Fink et al. colonial CWC have been obtained so far from the eastern
2013, 2015; Lo Iacono et al. 2014a, b; Stalder et al. 2015; basin and less than 20 from the SML province (Fig. 9.5b).
Wienberg and Titschack 2017; Wienberg, this volume). Data collected from the upper 3–4 m of the SML mounds
indicate the presence of up to ~1.5 m thick coral-dominated
.3.1.4 Late Pleistocene (Last 50 kyrs) - Holocene
9 deposits that, in the lower part, are rich in L. pertusa
Thanks to the recent increased interest in the study of sub- branches. The latter were dated back to a period ranging
merged CWC mounds and the large number of deep-sea from ~14 to ~11.5 kyr BP (McCulloch et al. 2010;
coral specimens dated using radiometric techniques, our Malinverno et al. 2010; Fink et al. 2012). Fink et al. (2012)
knowledge on Late Pleistocene and Holocene CWC has ascribed the absence of CWC during the Early to Mid-
highly improved in the last years. As summarised by Holocene, in two cores from the SML mounds, to low-oxy-
McCulloch et al. (2010) and Fink et al. (2015), and updated gen conditions (~2 ml l−1) estimated on the basis of the
by 28 coral ages later obtained by further investigation relative abundance of selected deep-infaunal foraminiferan
(Stalder et al. 2015; Titschack et al. 2016; Dubois-Dauphin species. These authors assumed moreover a direct relation-
et al. 2016, 2017), the oldest dated frame-building ship between the demise of CWC mound accretion in the
Mediterranean CWC specimens (L. pertusa) is around SML province, from 11.4 to 5.9 cal kyr BP, and the forma-
50 kyrs old (Fig. 9.4; Appendix 9.3). As underlined by Fink tion of the organic-rich sapropel S1 in deeper waters of the
et al. (2015), almost all coralla of L. pertusa and M. oculata eastern Mediterranean basin. Corals seem to re-appear in
the SML province around 6 kyr BP with the dominance of its known so far have been observed in the central and west-
M. oculata over L. pertusa (Malinverno et al. 2010), as ern side of the Mediterranean (Fig. 9.3). However these
typical of the modern Mediterranean Sea CWC communi- deposits are dominated by silt and clays and contain mostly
ties (Chimienti et al., this volume). soft-bottom corals (Vertino 2003). Instead, thanks to recent
Particularly interesting are the Late Pleistocene solitary regional strong uplifts, Early Pleistocene CWC paleo-habi-
CWC “micro-buildups”, known from ~1000 to well over tats abundantly crop out in the southeastern side of the
2000 m, such as (1) the Desmophyllum clusters encrusting Mediterranean, mostly in southern Italy and Greece (see
the Malta-Siracusa Escarpment (MSE) (Taviani and Sect. 9.3.1.3). According to Table 9.1, with exception of
Colantoni 1984; Delibrias and Taviani 1985) and rocky walls Dendrophyllia cornigera, the occurrences of all species
of the Sicily Strait (SS) (Vertino 2003) and (2) the examined herein is much higher in the Early Pleistocene than
Caryophyllia-Desmophyllum aggregations known offshore in the Miocene and Pliocene.
Crete (Taviani et al. 2011). The latter coral clusters are Extensive Atlantic-like CWC communities, dominated
formed by unusually large and thick-walled specimens of D. by L. pertusa, commonly associated with M. oculata, C.
dianthus and C. coronata (=sarsiae) (Fig. 9.2d) growing on coronata and E. scillae, were thriving in the Mediterranean
each other. D. dianthus is still living in several localities of during the Early Pleistocene. From around 1 million year
the modern Mediterranean (Altuna and Poliseno, this vol- up to ~ 50 kyr BP there is an important gap of information.
ume; Aymà et al., this volume; Chimienti et al., this volume; Almost nothing is known about CWC though ongoing stud-
Fourt et al., this volume; Lastras et al., this volume) and, as ies on coral mounds from the Alborán Sea hint at the estab-
shown in Fig. 9.4, has been more or less constantly present in lishing of the largest mounds in the Middle Pleistocene
this basin in the last 40 kyr. However, the Holocene and mod- (Krengel et al. 2017; Wienberg, this volume). Much more is
ern Desmophyllum morphotypes show a relatively small size known about the last 50 kyr though information on
and a much thinner wall than the “giant” ones from the MSE, Madrepora and Lophelia are almost completely lacking
SS and Crete. Moreover, they do not form aggregations with before the last 14 kyr (Fig. 9.4). According to Fink et al.
Caryophyllia coronata. The age of thick-walled (2015) these two species seem to have suddenly “(re-)
Desmophyllum from the MSE seems to be comprised appeared” in the Bølling- Allerød period in the
between 30 and 15 kyr BP (Taviani and Colantoni 1984; Mediterranean basin. However, although very rarely
Delibrias and Taviani 1985) and the only two ages available reported so far, Lophelia and Madrepora are known
for the species C. coronata (one of them collected as a between 50 and 15 kyr (Appendices 9.2 and 9.3; Fig. 9.4)
“micro-buildup” offshore Crete) fall within the same time
interval (16,600 ± 180, McCulloch et al. 2010 and ~26,000,
Zibrowius 1980). C. coronata is currently known as fossil in
the Mediterranean (Vertino 2003; Vertino and Corselli, this Table 9.1 Number of occurrences (= on-land sites) of the most com-
volume) but it is associated with the deep-sea Lophelia- mon extant frame-building deep-sea scleractinian species, and associ-
Madrepora-Desmophyllum communities of the NE Atlantic; ated solitary ones, from Miocene to Early Pleistocene deposits of
peri-mediterranean regions. Data from Appendix 9.1
it is quite common in the Porcupine Seabight at depth rang-
ing between 600 and 1000 m and temperature lower than Miocene Pliocene Early Pleistocene
10 °C (Vertino et al. 2015). Lophelia pertusaa 2 1 24
Madrepora oculataa 6 4 26
Desmophyllum dianthusb 2 2 18
Dendrophyllia cornigerab 13 7 11
9.4 patio-Temporal Patterns of Key
S Enallopsammia scillaeb 3 2 14
Cold-Water Coral Species (f)
Caryophyllia aradasianac 2? 1 8
The observations carried out so far on the spatio-temporal Caryophyllia coronatac 2? 0 11
distribution of the key species L. pertusa, M. oculata, D. (f)
Stenocyathus vermiformisc 0 1 14
dianthus, D. cornigera, E. scillae, C. aradasiana, C. coro-
nata and Stenocyathus vermiformis are summarised in (f): species known only as fossil (until the Late Pleistocene) in the
Mediterranean but still living in deep-sea environments of the NE
Figs. 9.3, 9.4, and 9.5 and, only regarding on-land outcrops, Atlantic Ocean
in Table 9.1. It should be noted that the values reported in a
Colonial species commonly fusing their skeletons; high frame-building
Table 9.1 have to be considered with caution because affected potential
by sampling bias and outcrop availability, especially regard-
b
Solitary gregarious and colonial species, the latter rarely fuse their
branches; moderate frame-building potential
ing the Pliocene (see Sect. 9.3.1.2). Considering the spatial c
Solitary species associated to frame-building CWC; no frame-building
distribution, most of the Miocene and Pliocene CWC depos- potential
in this basin. Moreover, most branches dated so far were Other temporal modifications can be observed consider-
collected in the upper 1–2 m of sediment. This means that, ing the species examined in this study. C. coronata and E.
based on the current available data, the presence of scillae, like other stenothermic bathyal species living today
Mediterranean Lophelia-Madrepora communities before exclusively in deep and cold (<10 °C) seafloors of the NE
the last deglaciation cannot be excluded. Atlantic, seem to have become extinct at the end of the
By combining all ages (last 50 kyr) of M. oculata and L. Pleistocene (Zibrowius 1987; Corselli 2001; Vertino 2003;
pertusa published thus far (Fig. 9.4), it is evident the highly Di Geronimo et al. 2005; Vertino and Corselli, this volume).
frequent occurrence of L. pertusa during the late Bølling- Moreover, circalittoral-bathyal species, such as C. arada-
Allerød, the early Younger Dryas and in the Early Holocene. siana (= calveri) and S. vermiformis have become more
The distribution and number of coral ages (Fig. 9.4), con- common in association with frame-building CWC in the
firmed by observations carried out on sediment cores from Holocene (Vertino pers. observ.). In particular, C. calveri is
both eastern and western Mediterranean coral mounds always associated with modern Madrepora-Lophelia-
(Malinverno et al. 2010; Stalder et al. 2015; Fink et al. Desmophyllum communities of the Mediterranean (e.g.
2012, 2013, 2015), indicate “switches” in the dominance of Altuna and Poliseno, this volume; Rueda et al., this volume)
the most common frame-building coral species (L. pertusa and seems to have occupied the ecological niche inhabited
vs M. oculata). This is particularly evident after ~10 kyr BP by C. coronata in the Pleistocene (and still today in the NE
in the western Mediterranean, when Lophelia underwent a Atlantic). The extinction of stenothermic bathyal species in
sharp demise. After this age, though suffering temporary the Mediterranean has been explained by several authors
declines, M. oculata became the dominant species of the with the shift from psychrosphere to thermosphere condi-
Mediterranean and it remains so to this day (e.g. Taviani tions of the Mediterranean Sea, as a consequence of the tran-
et al. 2005a; Freiwald et al. 2009; Vertino et al. 2010; Gori sition from glacial to interglacial age (Benson 1972; Russo
et al. 2013; Fourt et al. 2017). This compositional change in 1980; Di Geronimo et al. 1996; Corselli 2001). This is in
CWC, corresponding to a remarkable decrease in mound agreement with the two available ages of C. coronata
accretion rate in the Alboran Sea (Wienberg, this volume), (Fig. 9.4) and to the ages of coral clusters formed by this spe-
has been explained by Stalder et al. (2015) with the better cies and “giant” Desmophyllum (Delibrias and Taviani 1985;
tolerance of M. oculata to higher temperature and unstable Taviani et al. 2011). However, further CWC dating is needed
environmental conditions established at the Pleistocene- to confirm this hypothesis (see Vertino and Corselli, this
Holocene boundary. This coral switch is observable also in volume).
the eastern Mediterranean where the decline of L. pertusa In modern CWC habitats, coral accretion and sediment
seems to occur earlier. However the low number of coral accumulation is highly influenced by local environmental
ages obtained so far does not allow to draw robust conclu- changes, such as micro-current regimes (see Hayes et al.,
sions in this part of the basin. The occurrence of L. pertusa this volume). This makes these environments extremely
in the Holocene could be overestimated because the thick heterogeneous at spatial scale, even within few meters,
skeleton of this species is generally preferred to the thinner and the reconstruction of their evolution through time
one of Madrepora for radiometric dating. very complex to be determined based on limited samples.
The comparison between ages of Lophelia and Madrepora A very large amount of fossil data is needed to put for-
specimens specifically collected from CWC mounds located ward robust hypotheses about modifications of CWC
in the western and eastern Mediterranean (Fig. 9.5a, b), high- abundance and composition through time in relation to
lights a similar distributional trend. The wider gap observed broad-scale environmental changes. For instance, the high
in the eastern basin in the Early and Mid-Holocene should be number of Lophelia occurrences in the Early Holocene
ascertained with the analysis of additional samples, but the (especially in the western Mediterranean), reported in
hypothesis of a direct relation with the sapropel S1, put for- recent studies (e.g. McCulloch et al. 2010; Fink et al.
ward by Fink et al. (2012), seems at the moment the most 2015) and summarised herein, seem to contradict the pre-
plausible explanation. Due to the larger number of speci- vious general hypothesis of frame-building CWC demise
mens, the lack of corals between ~9 and 6 kyr observed in during deglacial periods. Moreover, the inference by Fink
the western Mediterranean mounds (Fig. 9.5a, see also et al. (2015) regarding the “pronounced 1,400-yrs-lasting
Wienberg, this volume) is more reliable and has been gap in the occurrence of L. pertusa” during the YD in the
explained by Fink et al. (2015) as a consequence of the Alborán basin has been denied by the almost contempora-
decrease of productivity at the onset of the Mid-Holocene, neous study carried out by Stalder et al. (2015) that has
resulting in a more oligotrophic regime in the western basin ascertained the presence of this species in the YD by
(Bárcena et al. 2001; Cacho et al. 2002; Jimenez-Espejo dating additional specimens.
et al. 2008; Fink et al. 2013).
9.5 onclusive Remarks and Future

C volume). As to the last 50 kyr, the spatio-temporal distribu-
Perspectives tion of D. dianthus, L. pertusa and M. oculata appears to be
quite different (Fig. 9.4; Appendices 9.2 and 9.3). Thirteen
The data compilation presented in this chapter includes occurrences of D. dianthus have been reported before the B /
information on the most important frame-building species of A period, between around 39 and 14.6 kyr BP and most of
the Mediterranean since the Miocene. It clearly depicts the them are referred to thick-walled specimens, locally associ-
profound changes overcome by CWC in the highly dynamic ated to C. coronata, collected at depth higher than 1000 m.
Mediterranean basin (Taviani 2002), in response to a variety Instead only 2 of the 50 dated specimens of M. oculata and 4
of mutating oceanographic and climatic scenarios. As dis- of the 78 dated ones of L. pertusa have resulted to be older
closed by precise dating in the Late Pleistocene-Holocene, than the Bølling-Allerød interstadial (B/A). This species-
important demise or recolonisation events can take place specific temporal distribution pattern can be real, thus reflect-
even at short temporal scales (less than 103), almost impos- ing the absence of the two colonial species before the B/A, or
sible to discriminate in older situations. affected by a selection sampling bias due to the fact that in the
This chapter highlights the improved knowledge gained Mediterranean both live and dead/fossil Desmophyllum is
on Late Pleistocene CWC through radiometric dating of over more common on walls and overhangs (Aymà et al., this vol-
150 coral specimens (Appendices 9.2 and 9.3; Fig. 9.4), but ume; Lastras et al., this volume) than the other two species.
it also calls attention to the need for further studies, espe- All Desmophyllum specimens older than 14 kyr were indeed
cially on older coral occurrences, to properly interpret modi- collected through rock dredging along escarpments where,
fications through geological time. For several exceptional due to little sediment accumulation, it is likely to find very old
Neogene and Quaternary on-land CWC sites, further taxo- specimens still exposed on the surface or covered by a thin
nomic, paleoecological and chronostratigraphic data are still muddy drape. The same is true also for the four specimens of
required. Additionally, with exception of the outcrops from Lophelia and Madrepora older than 14 kyr that were in fact
southern Italy (recently accurately mapped) precise locations collected through rock dredging (Appendices 9.2 and 9.3).
of most outcrops are still lacking. Instead, only specimens younger than 14 kyr were obtained
The hypothesis put forward by Vertino et al. (2014) through grabbing, box-coring or gravity coring (shorter than
about a major modification underwent by azooxanthellate 5 m) from coral mounds (Appendices 9.2 and 9.3). This
coral fauna at the Pliocene – Pleistocene boundary gets fur- means that it is more likely to collect Desmophyllum older
ther support by the increase of Atlanto-Mediterranean spe- than 14 kyr than Lophelia or Madrepora and that further sam-
cies (L. pertusa, M. oculata, D. dianthus, E. scillae, C. pling effort is needed to verify the actual absence of these two
aradasiana and C. coronata) shown in Table 9.1. Thus far, colonial corals before the B/A interstadial, apparently ascer-
truly CWC bioconstructions (Lophelia-Madrepora domi- tained in the western basin (Wienberg, this volume).
nated), comparable to the modern ones, have not been Interestingly, all thick-walled and large Desmophyllum
recorded in Miocene deposits. The only CWC buildups specimens as well as Desmophyllum-Caryophyllia coronata
known in this epoch are dominated by dendrophylliid cor- aggregations collected so far at depth higher than 1000 m
als (Mastandrea et al. 2002; Vescogni et al. 2018). The seem to have disappeared with the end of the last glacial
presence of L. pertusa has been ascertained in the Upper period. This basin-scale extinction at the Pleistocene-
Pliocene Marmorito bioconstructions, dominated by Holocene boundary is coeval to the disappearance from the
Enallopsammia and Desmophyllum, but in these limestones Mediterranean of several Atlantic stenothermic bathyal spe-
Lophelia occurs only as a secondary component. On the cies belonging to cnidarians, molluscs, bryozoans, serpulids
basis of the data collected so far, there is no evidence of etc. (Di Geronimo et al. 1996, 2005; Vertino 2003; Vertino
Lophelia-dominated bioconstructions before the Calabrian et al. 2014). This bathyal species impoverishment could be
stage when, as testified by the remarkable fossil CWC leg- explained as the direct consequence of temperature increase
acy of southern Italy, the branching frame-building coral in the deep sea or, more likely, as the indirect effect of more
was associated to several Atlantic stenothermic bathyal complex oceanographic modifications occurred at the gla-
species belonging to the order Scleractinia (such as C. cor- cial-interglacial transition (Vertino and Corselli, this
onata, E. scillae) and to several other taxonomic groups (Di volume).
Geronimo et al. 1996; Vertino 2003). As for the last 14 kyr, the data collection presented herein
Our analysis points out a significant gap in knowledge on combined with observations performed on sediment cores
Mediterranean CWC for the long time interval period com- (Malinverno et al. 2010; Stalder et al. 2015; Wienberg, this
prised between ~1 million year (younger emerged CWC out- volume) hint at a “golden age” of L. pertusa as frame-
crop) and 50 kyr ago. This gap is going to be partly solved by building coral until ~11 and ~10 kyr BP in the eastern and
the study of drilled submerged coral mounds (Wienberg, this western Mediterranean, respectively (Figs. 9.4 and 9.5). The
end of the flourishing Lophelia period is concurrent with research field. His endless enthusiasm has been the motor of the
COCARDE-ERN (European Research Network) programme, funded
lowered mound accretion rates (Wienberg, this volume) and by the European Science Foundation, from which the study presented
the subsequent general demise (until around 6 kyr BP) of herein greatly benefited. This research is also part of EU F.P. VII
CWC bioconstructors from Mediterranean mound provinces Projects COCONET, (contract no. 287844), and EVER-EST (contract
(Figs. 9.4 and 9.5). This has been explained with the concur- no. 674907), DG Environment programme IDEM (grant agreement
No 11.0661 /2017/750680/SUB/EN V.C2), and the Flag Project
rent formation of sapropel S1 in the eastern basin (Fink et al. Ritmare (Ricerca Italiana per il Mare) project, and is Ismar-Bologna
2012) and productivity decrease/unstable environmental scientific contribution n. 1938. We are very grateful to Fabio Marchese
conditions in the western one (Fink et al. 2013, 2015; Stalder for providing the georeferenced map of the Mediterranean used as
et al. 2015; Wienberg, this volume). However, further analy- background in Fig. 9.3. We warmly thank Lydia Beuck, Francesca
Bosellini, Italo Di Geronimo, André Freiwald, Juergen Titschack,
ses are needed to define the exact age of development and Alessandro Vescogni and Helmut Zibrowius for constructive discus-
decline phases of Mediterranean frame-building CWC and sions on the evolution of modern and ancient Mediterranean deep-sea
to put forward robust conclusions on their modifications coral environments. We are moreover grateful to Antonietta Rosso,
through time. Italo Di Geronimo, Francesca Bosellini, Enzo Burgio, Daniele
Ormezzano, Paolo Serventi for help in accessing the fossil scleractin-
The high intraspecific variability and phenotypic plas- ian historical collections in the following Italian repositories: Museum
ticity of scleractinians has recurrently caused the misiden- of Paleontology, University of Catania, Museum of Paleobiology and
tification of colonial fragments belonging to the same Botanical Garden, University of Modena and Reggio Emilia,
species, or even to the same specimen, as distinct taxa. This “G. Gemmellaro” Museum of Palaeontology and Geology, University
of Palermo, Museum of Natural History, Torino University. Marco
is particularly true for ancient papers focused on fossil Sami, Vincenzo Bugnano and Massimo Rocca kindly made available
assemblages often composed by few well preserved corals to us a number of Neogene scleractinians. Paolo Montagna and Tim
and mostly preserved as small fragments. The arbitrary Collart are warmly thanked for useful suggestions regarding the treat-
establishment of new species, based on rare, poorly pre- ment of 14C coral datings. Last but not least, special thanks go to the
editors (Covadonga Orejas and Carlos Jiménez) and the reviewers
served and fragmented specimens, combined with the poor (Antonietta Rosso and Jarek Stolarski) who provided constructive
knowledge of the intraspecific variability of modern deep- criticism that helped us to improve the manuscript.
sea corals, have generated through time the development of
a huge number of unreliable (morpho)species names.
Therefore, coral occurrences obtained from the literature
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Drop Chapter
Bathyal Corals Within the Aegean Sea 10
and the Adjacent Hellenic Trench
Jürgen Titschack
Abstract Twenty-seven scleractinian species, two of which zooxan-

Within the Aegean Sea and the adjacent Hellenic trench, thellate, have been documented so far from the Aegean Sea
128 records of bathyal corals (>200 m water depth; only and the adjacent Hellenic trench in the eastern Mediterranean
6% recorded alive) are described so far, comprising 13 (Zibrowius 1979, 1987; Vafidis et al. 1997; Morri et al. 2000;
species. Further fossil occurrences of these corals are Gerovasileiou et al. 2009, 2015; Salomidi et al. 2010, 2013;
documented from 10 outcrops on Crete and Rhodes. Taviani et al. 2011; Çinar et al. 2014). Among these, 13 spe-
Caryophyllia calveri, Caryophyllia sarsiae, Dendrophyllia cies have been reported from bathyal water depths (exceed-
cornigera, Desmophyllum dianthus, Javania cailleti, ing 200 m; Fig. 10.1a). From a total of 128 findings in bathyal
Lophelia pertusa, Madrepora oculata, Schizocyathus fis- depths, only 8 records refer to living corals comprising spec-
silis, Stenocyathus vermiformis and Trochocyathus medi- imens of Caryophyllia smithii Stokes and Broderip, 1828,
terraneus predominate in water depths >200 m. Although Dendrophyllia cornigera (Lamarck, 1816), Stenocyathus
Caryophyllia smithii, Guynia annulata and Paracyathus vermiformis (Pourtalès, 1868) and Desmophyllum dianthus
pulchellus also occur in deeper waters, they are mainly (Esper, 1794) (see also Fig. 10.1a; Table 10.1; see Altuna and
reported from shallower water depths. Radiogenic dates Poliseno, this volume). All other reports refer to dead speci-
obtained from various deep-water species imply their mens or to specimens of which the status is not entirely clear.
presence in this region since the mid-Pleistocene, how- Caryophyllia calveri Duncan, 1873, Caryophyllia sarsiae
ever most dates exhibit ages since the last glacial maxi- Zibrowius, 1974, D. cornigera, D. dianthus, Javania cailleti
mum. All bathyal coral species are predominantly found (Duchassaing and Michelotti, 1864), Lophelia pertusa
on steep escarpments and topographic highs in coarse (Linnaeus, 1758), Madrepora oculata Linnaeus, 1758, pre-
sediments or on hard substrates along the steep structured dominate in water depths >200 m; Schizocyathus fissilis
slope of the Hellenic Trench off Crete, Karpathos and Pourtalès, 1874, S. vermiformis and Trochocyathus mediter-
Rhodes. A similar environment setting is reconstructed raneus Zibrowius, 1980, are only reported from water depths
for the fossil occurrences on Rhodes. >400 m (Table 10.1). Caryophyllia smithii, Guynia annulata
Duncan, 1872 and Paracyathus pulchellus (Philippi, 1842)
Keywords are only rarely reported from bathyal water depths (6 records)
Bathyal corals · Cold-water corals · Aegean Sea · but occur frequently in water depths <200 m (35 records; 24
Hellenic trench · Eastern Mediterranean Sea living, not indicated in Fig. 10.1a). Only L. pertusa, M. ocu-
lata and D. cornigera are colonial. L. pertusa, M. oculata
and D. dianthus form the white coral community or
‘Biocoenose des coraux blanc’, well-known from the entire
Mediterranean Sea (sensu Pérès and Picard 1964; Freiwald
et al. 2009; see Altuna and Poliseno, this volume; Chimienti
et al., this volume).
J. Titschack (*) All bathyal coral species are predominantly found along
MARUM – Center for Marine Environmental Sciences, the eastern Hellenic Arc off Crete, Karpathos and Rhodes
Bremen, Germany within the northern Levantine Sea (Taviani et al. 2011). This
SaM – Senckenberg am Meer Wilhelmshaven, Abteilung region is characterised by steep slopes that are highly struc-
Meeresforschung, Wilhelmshaven, Germany tured by submarine canyons (Fig. 10.1a; Harris and Whiteway

https://doi.org/10.1007/978-3-319-91608-8_10
86 J. Titschack
colonial solitary
Lophelia pertusa Paracyathus pulchellus Desmophyllum dianthus Javania cailleti
Madrepora oculata Caryophyllia smithii Caryophyllia sarsiae Schizocyathus fissilis
Dendrophyllia cornigera Guynia annulata Caryophyllia calveri Trochocyathus mediterraneus
<200 mwd records Stenocyathus vermiformis live occurrences
b Lophelia pertusa
Madrepora oculata
Desmophyllum dianthus
Caryophyllia sarsiae
Caryophyllia calveri
Stenocyathus vermiformis
Sapropel S1
0 10 20 30 650 700 750 800

Age [ka BP]
c
Framework-forming
baythal corals
Coral deposits
Hemipelagic sediments
Basement rock
Fig. 10.1 (a) Map of the Aegean Sea and the adjacent Hellenic data sources see text). (c) Palaeoenvironmental reconstruction of
trench. All bathyal coral occurrences are indicated (red symbol Rhodesian bathyal coral occurrences. Bathyal coral deposits form
boundaries indicate living occurrences; for data see Table 10.1). predominately at the base of the steep palaeorelief as debris flow (1)
White lines indicate canyons (Harris and Whiteway 2011). and debris fall (2) deposits. (Modified after Titschack and Freiwald
Bathymetry: http://www.emodnet.eu/bathymetry. (b) Available coral 2005; outcrop positions indicated in map; for data sources see
ages from the study area. Duration of Sapropel S1 is indicated (for Table 10.2)
Table 10.1 Records of bathyal corals within the Aegean Sea and the adjacent Hellenic trench compiled from various sources
Area Station Gear Latitude [°N] Longitude [°E] Depth [m] CoralSpecies Facies Status Reference
Off Milos – 36.6417 24.4613 90 Caryophyllia smithii On oceanographic Live Morri et al. (2000)
instrument
SSW of Chryssi Island – 34.8330 25.7020 520–620 Dendrophyllia cornigera RB, C rubble Live Smith et al. (2009)
SE of Crete GECO-56 D 35.0022 26.2972 378–773 ?Desmophyllum Gravel/Breccia Dead Taviani et al. (2011)
NE of Rhodes GECO-89 G 36.3607 28.2807 328–376 Caryophyllia calveri L-M rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-84 D 35.8298 27.9277 354–753 Caryophyllia calveri Den rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-84 D 35.8298 27.9277 354–753 Caryophyllia calveri C rubble Unknown Taviani et al. (2011)
E of Crete GECO-55 D 35.1277 26.4685 366–647 Caryophyllia calveri Den rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-85 D 35.8323 27.9262 403–762 Caryophyllia calveri L-M rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-85 D 35.8323 27.9262 403–762 Caryophyllia calveri C rubble Unknown Taviani et al. (2011)
S of Karpathos GECO-22 G 35.4167 27.2247 453–455 Caryophyllia calveri L-M rubble Unknown Taviani et al. (2011)
S of Karpathos GECO-18 D 35.4123 27.2233 453–550 Caryophyllia calveri L-M rubble Dead Taviani et al. (2011)
S of Karpathos GECO-28 G 35.4175 27.2248 460–461 Caryophyllia calveri L-M rubble Unknown Taviani et al. (2011)
SE of Rhodes GECO-77 G 35.8330 27.9215 465–506 Caryophyllia calveri L-M rubble Unknown Taviani et al. (2011)
SE of Rhodes GECO-80 G 35.8300 27.9225 477–482 Caryophyllia calveri Stenocyathus rubble Unknown Taviani et al. (2011)
SE of Rhodes GECO-82 G 35.8193 27.9128 493–507 Caryophyllia calveri ? Dead Taviani et al. (2011)
S of Crete GECO-50 D 34.7637 25.1142 1408–2133 Caryophyllia sarsiae Des-C framestone Dead Taviani et al. (2011)
10 Bathyal Corals in the Aegean Sea and the Hellenic Trench
SE of Rhodes GECO-76 D 35.5623 27.9825 1445–2268 Caryophyllia sarsiae Des-C framestone Dead Taviani et al. (2011)
SE of Rhodes GECO-64 D 35.8353 27.9618 1458–1963 Caryophyllia sarsiae Des-C framestone Dead Taviani et al. (2011)
SE of Crete GECO-54 D 34.7368 26.1187 1741–2179 Caryophyllia sarsiae Des-C framestone Dead Taviani et al. (2011)
S of Karpathos GECO-21 G 35.4138 27.2243 451–452 Caryophyllia sarsiae L-M rubble Dead Taviani et al. (2011)
E of Rhodes GECO-75 D 36.0252 28.1510 922–1640 Caryophyllia sarsiae Des-C framestone Dead Taviani et al. (2011)
SE of Rhodes GECO-84 D 35.8298 27.9277 354–753 Dendrophyllia cornigera Den rubble Dead Taviani et al. (2011)
E of Crete GECO-55 D 35.1277 26.4685 366–647 Dendrophyllia cornigera Den rubble Dead Taviani et al. (2011)
S of Karpathos GECO-22 G 35.4167 27.2247 453–455 Dendrophyllia cornigera L-M rubble Dead Taviani et al. (2011)
S of Karpathos GECO-28 G 35.4175 27.2248 460–461 Dendrophyllia cornigera L-M rubble Dead Taviani et al. (2011)
S of Crete GECO-50 D 34.7637 25.1142 1408–2133 Desmophyllum dianthus Des-C framestone Dead Taviani et al. (2011)
SE of Rhodes GECO-76 D 35.5623 27.9825 1445–2268 Desmophyllum dianthus Des-C framestone Dead Taviani et al. (2011)
SE of Rhodes GECO-64 D 35.8353 27.9618 1458–1963 Desmophyllum dianthus Des-C framestone Dead Taviani et al. (2011)
SE of Crete GECO-54 D 34.7368 26.1187 1741–2179 Desmophyllum dianthus Des-C framestone Dead Taviani et al. (2011)
SE of Rhodes GECO-79 G 35.8353 27.9113 284–284 Desmophyllum dianthus L-M rubble Dead Taviani et al. (2011)
NE of Rhodes GECO-89 G 36.3607 28.2807 328–376 Desmophyllum dianthus L-M rubble Dead Taviani et al. (2011)
E of Crete GECO-55 D 35.1277 26.4685 366–647 Desmophyllum dianthus Den rubble Dead Taviani et al. (2011)
SE of Crete GECO-56 D 35.0022 26.2972 378–773 Desmophyllum dianthus N-Des framestone Dead Taviani et al. (2011)
SE of Rhodes GECO-85 D 35.8323 27.9262 403–762 Desmophyllum dianthus L-M rubble Dead Taviani et al. (2011)
W of Crete GECO-7 D 35.5688 23.3072 426–968 Desmophyllum dianthus N-Des framestone Unknown Taviani et al. (2011)
S of Karpathos GECO-21 G 35.4138 27.2243 451–452 Desmophyllum dianthus L-M rubble Dead Taviani et al. (2011)
S of Karpathos GECO-22 G 35.4167 27.2247 453–455 Desmophyllum dianthus L-M rubble Unknown Taviani et al. (2011)
S of Karpathos GECO-18 D 35.4123 27.2233 453–550 Desmophyllum dianthus M-L rudstone Dead Taviani et al. (2011)
S of Karpathos GECO-18 D 35.4123 27.2233 453–550 Desmophyllum dianthus L-M rubble Dead Taviani et al. (2011)
(continued)
87
Table 10.1 (continued)
88
S of Karpathos GECO-28 G 35.4175 27.2248 460–461 Desmophyllum dianthus L-M rubble Unknown Taviani et al. (2011)
SE of Rhodes GECO-77 G 35.8330 27.9215 465–506 Desmophyllum dianthus M-L rudstone Dead Taviani et al. (2011)
SE of Rhodes GECO-77 G 35.8330 27.9215 465–506 Desmophyllum dianthus L-M rubble Unknown Taviani et al. (2011)
SE of Rhodes GECO-80 G 35.8300 27.9225 477–482 Desmophyllum dianthus L-M rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-81 G 35.8190 27.9147 496–510 Desmophyllum dianthus – Dead Taviani et al. (2011)
W of Crete GECO-8 D 35.5603 23.4488 743–1334 Desmophyllum dianthus N-Des framestone Unknown Taviani et al. (2011)
SE of Crete GECO-41 D 34.9475 26.2158 761–781 Desmophyllum dianthus Gravel/Breccia Dead Taviani et al. (2011)
E of Rhodes GECO-75 D 36.0252 28.1510 922–1640 Desmophyllum dianthus Des-C framestone Dead Taviani et al. (2011)
S of Karpathos GECO-36 rd 35.5260 27.2233 126–142 Guynia annulata Fine sed. with Dead Taviani et al. (2011)
octocoral axes
S of Crete GECO-13 G 34.9987 23.9755 219–226 Guynia annulata Fine sed. with Unknown Taviani et al. (2011)
octocoral axes
SE of Rhodes GECO-79 G 35.8353 27.9113 284–284 Guynia annulata L-M rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-85 D 35.8323 27.9262 403–762 Javania cailleti L-M rubble Dead Taviani et al. (2011)
S of Karpathos GECO-18 D 35.4123 27.2233 453–550 Javania cailleti L-M rubble Dead Taviani et al. (2011)
NE of Rhodes GECO-90 G 36.3665 28.3247 1208–1208 Lophelia pertusa L-M rubble Dead Taviani et al. (2011)
NE of Rhodes GECO-89 G 36.3607 28.2807 328–376 Lophelia pertusa L-M rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-84 D 35.8298 27.9277 354–753 Lophelia pertusa Den rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-85 D 35.8323 27.9262 403–762 Lophelia pertusa M-L rudstone Dead Taviani et al. (2011)
SE of Rhodes GECO-85 D 35.8323 27.9262 403–762 Lophelia pertusa L-M rubble Dead Taviani et al. (2011)
W of Crete GECO-7 D 35.5688 23.3072 426–968 Lophelia pertusa N-Des framestone Dead Taviani et al. (2011)
S of Karpathos GECO-33 D 35.4370 27.2388 450–450 Lophelia pertusa L-M rubble Dead Taviani et al. (2011)
S of Karpathos GECO-21 G 35.4138 27.2243 451–452 Lophelia pertusa L-M rubble Dead Taviani et al. (2011)
S of Karpathos GECO-18 D 35.4123 27.2233 453–550 Lophelia pertusa M-L rudstone Dead Taviani et al. (2011)
S of Karpathos GECO-18 D 35.4123 27.2233 453–550 Lophelia pertusa L-M rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-77 G 35.8330 27.9215 465–506 Lophelia pertusa M-L rudstone Dead Taviani et al. (2011)
SE of Rhodes GECO-77 G 35.8330 27.9215 465–506 Lophelia pertusa L-M rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-80 G 35.8300 27.9225 477–482 Lophelia pertusa L-M rubble Dead Taviani et al. (2011)
NE of Rhodes GECO-90 G 36.3665 28.3247 1208–1208 Madrepora oculata L-M rubble Dead Taviani et al. (2011)
S of Karpathos GECO-29 D 35.4157 27.2267 173–521 Madrepora oculata M-L rudstone Dead Taviani et al. (2011)
S of Karpathos GECO-29 D 35.4157 27.2267 173–521 Madrepora oculata L-M rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-79 G 35.8353 27.9113 284–284 Madrepora oculata M-L rudstone Dead Taviani et al. (2011)
SE of Rhodes GECO-79 G 35.8353 27.9113 284–284 Madrepora oculata L-M rubble Dead Taviani et al. (2011)
NE of Rhodes GECO-89 G 36.3607 28.2807 328–376 Madrepora oculata L-M rubble Dead Taviani et al. (2011)
SE of Rhodes GECO-85 D 35.8323 27.9262 403–762 Madrepora oculata M-L rudstone Dead Taviani et al. (2011)
SE of Rhodes GECO-85 D 35.8323 27.9262 403–762 Madrepora oculata L-M rubble Dead Taviani et al. (2011)
S of Karpathos GECO-21 G 35.4138 27.2243 451–452 Madrepora oculata L-M rubble Dead Taviani et al. (2011)
J. Titschack
S of Karpathos GECO-18 D 35.4123 27.2233 453–550 Madrepora oculata M-L rudstone Dead Taviani et al. (2011)
SE of Rhodes GECO-77 G 35.8330 27.9215 465–506 Madrepora oculata M-L rudstone Dead Taviani et al. (2011)
S of Crete GECO-13 G 34.9987 23.9755 219–226 Paracyathus pulchellus Fine sed. with Unknown Taviani et al. (2011)
octocoral axes
SE of Rhodes GECO-83 G 35.7827 27.8508 1119–1125 Schizocyathus fissilis Fine sed. with Unknown Taviani et al. (2011)
octocoral axes
NE of Rhodes GECO-90 G 36.3665 28.3247 1208–1208 Stenocyathus vermiformis L-M rubble Dead Taviani et al. (2011)
S of Crete GECO-13 G 34.9987 23.9755 219–226 Stenocyathus vermiformis Fine sed. with Unknown Taviani et al. (2011)
octocoral axes
SE of Rhodes GECO-79 G 35.8353 27.9113 284–284 Stenocyathus vermiformis L-M rubble Unknown Taviani et al. (2011)
NE of Rhodes GECO-89 G 36.3607 28.2807 328–376 Stenocyathus vermiformis L-M rubble Unknown Taviani et al. (2011)
SE of Rhodes GECO-84 D 35.8298 27.9277 354–753 Stenocyathus vermiformis Den rubble Dead Taviani et al. (2011)
E of Crete GECO-55 D 35.1277 26.4685 366–647 Stenocyathus vermiformis S rubble Unknown Taviani et al. (2011)
SE of Rhodes GECO-85 D 35.8323 27.9262 403–762 Stenocyathus vermiformis L-M rubble Unknown Taviani et al. (2011)
S of Karpathos GECO-33 D 35.4370 27.2388 450–450 Stenocyathus vermiformis L-M rubble Unknown Taviani et al. (2011)
S of Karpathos GECO-21 G 35.4138 27.2243 451–452 Stenocyathus vermiformis L-M rubble Dead Taviani et al. (2011)
S of Karpathos GECO-22 G 35.4167 27.2247 453–455 Stenocyathus vermiformis L-M rubble Unknown Taviani et al. (2011)
S of Karpathos GECO-18 D 35.4123 27.2233 453–550 Stenocyathus vermiformis L-M rubble Unknown Taviani et al. (2011)
S of Karpathos GECO-28 G 35.4175 27.2248 460–461 Stenocyathus vermiformis L-M rubble Unknown Taviani et al. (2011)
SE of Rhodes GECO-77 G 35.8330 27.9215 465–506 Stenocyathus vermiformis L-M rubble Unknown Taviani et al. (2011)
SE of Rhodes GECO-80 G 35.8300 27.9225 477–482 Stenocyathus vermiformis S rubble Unknown Taviani et al. (2011)
SE of Rhodes GECO-82 G 35.8193 27.9128 493–507 Stenocyathus vermiformis ? Dead Taviani et al. (2011)
SE of Crete GECO-48 D 34.9125 25.0668 630–680 Stenocyathus vermiformis Fine sed. with Unknown Taviani et al. (2011)
octocoral axes
SE of Crete GECO-41 D 34.9475 26.2158 761–781 Stenocyathus vermiformis Gravel/Breccia Dead Taviani et al. (2011)
S of Crete GECO-50 D 34.7637 25.1142 1408–2133 Trochocyathus Des-C framestone Dead Taviani et al. (2011)
mediterraneus
SE of Rhodes GECO-64 D 35.8353 27.9618 1458–1963 Trochocyathus Des-C framestone Dead Taviani et al. (2011)
mediterraneus
SE of Crete GECO-54 D 34.7368 26.1187 1741–2179 Trochocyathus Des-C framestone Dead Taviani et al. (2011)
mediterraneus
E of Rhodes GECO-75 D 36.0252 28.1510 922–1640 Trochocyathus Des-C framestone Dead Taviani et al. (2011)
mediterraneus
SE of Crete GECO-41 D 34.9475 26.2158 761–781 Undetermined Gravel/Breccia Unknown Taviani et al. (2011)
Caryophylliidae
Akrotiri Athos Stat. 139a T 40.1310 24.3850 180–200 Desmophyllum dianthus – Unknown Vafidis et al. (1997)
Off Limenaria Thasos Stat. 168b T 40.4570 24.5990 300–350 Lophelia pertusa – Unknown Vafidis et al. (1997)
I.
(continued)
89
90
Off Limenaria Thasos Stat. 168b T 40.4570 24.5990 300–350 Madrepora oculata – Unknown Vafidis et al. (1997)
I.
SE of Lesvos Stat. 200b trawl 38.9390 26.6050 70–90 Paracyathus pulchellus Maerl Unknown Vafides et al. (1997)
S of Karpathos 75/D40 – 35.0200 27.1383 600 Caryophyllia calveri – Dead Zibrowius (1979)
SE of Kastellórizon SME 1014 – 36.0694 29.6833 366–381 Caryophyllia calveri Yellowish fine sed. Dead Zibrowius (1979)
NW of Thira SME 765 – 36.4417 25.4000 375–394 Caryophyllia calveri Fine ash Dead Zibrowius (1979)
NE Gulf of SME 1538 – 39.3000 23.1083 55–62 Caryophyllia smithii Yellowish grey sand Live Zibrowius (1979)
Pagasitikos
Knimis channel SME 1533 – 38.7917 22.8250 58–61 Caryophyllia smithii Muddy gravel Live Zibrowius (1979)
N Euboean Gulf SME 1529 – 38.7117 23.1250 62 Caryophyllia smithii Grey muddy sand Live Zibrowius (1979)
NW Gulf of SME 1560 – 40.2056 23.4153 73 Caryophyllia smithii Slightly sandy mud Unknown Zibrowius (1979)
Cassandra
S of Paros SME 835 – 36.9181 25.1806 88 Caryophyllia smithii Coralligène Live Zibrowius (1979)
Betw. Paros and SME 836 – 36.9139 25.1028 100–102 Caryophyllia smithii Coralligène Unknown Zibrowius (1979)
Antiparos
Off Cape Cassandra SME 1564 – 39.9290 23.3400 100 Caryophyllia smithii Grey mud Unknown Zibrowius (1979)
Gulf of Kalamata SME 728 – 36.9917 22.1083 110 Caryophyllia smithii Coarse detritic sed. Dead Zibrowius (1979)
NW of Cape of SME 715 – 36.4306 22.4236 115–120 Caryophyllia smithii Coarse detritic sed. Dead Zibrowius (1979)
Matapan
S of Syros SME 814 – 37.2889 24.8694 115 Caryophyllia smithii HG Live Zibrowius (1979)
NW of Cape of SME 721 – 36.3889 22.4528 120–137 Caryophyllia smithii Coarse detritic sed. Live Zibrowius (1979)
Matapan
Betw. Syros and SME 843 – 37.2583 24.8375 160 Caryophyllia smithii HG and sandy-muddy Live Zibrowius (1979)
Serfopoula sed.
NE Crete 67/9 – 35.2333 26.3333 180 Caryophyllia smithii Muddy sand with Dead Zibrowius (1979)
biogenic elements
Betw. Alonnisos and SME 1545 – 39.3069 23.9958 185 Caryophyllia smithii Muddy sand Live Zibrowius (1979)
Kira Panagia
SE plane off Cape SME 792 – 38.1667 24.6278 300 Caryophyllia smithii Light grey fine sed. Dead Zibrowius (1979)
Kalireas
Betw. Panagia and SME 1544 – 39.3139 23.9911 200–270 Caryophyllia smithii Muddy coarse sand Live Zibrowius (1979)
Alonissos
SW of Antpsara SME 805 – 38.5056 24.4750 420 Dendrophyllia cornigera HG Live Zibrowius (1979)
S of Karpathos 75/D40 – 35.0200 27.1383 600 Dendrophyllia cornigera – Live Zibrowius (1979)
Betw. Panagia and SME 1544 – 39.3139 23.9911 200–270 Dendrophyllia cornigera Muddy coarse sand Live Zibrowius (1979)
Alonissos
N Euboean Gulf SME 1525 – 38.5367 23.5183 230–275 Desmophyllum dianthus – Live Zibrowius (1979)
W of Thira 67/61 – 36.4300 25.3260 60 Guynia annulata Seafloor with Dead Zibrowius (1979)
concretions of calc.
algae
Gulf of Kalamata SME 731 – 36.7517 22.0042 82–91 Guynia annulata Coarse detritic sed. Live Zibrowius (1979)
NE Crete 67/9 – 35.2333 26.3333 180 Guynia annulata Muddy sand with Dead Zibrowius (1979)
biogenic elements
J. Titschack
Strait of Kasos SME 747 – 35.2000 26.6500 180 Guynia annulata Muddy detrtic sed. Live Zibrowius (1979)
with rarely calc. algae
SE of Kastellórizon SME 1014 – 36.0694 29.6833 366–381 Lophelia pertusa Yellowish fine sed. Dead Zibrowius (1979)
SE of Kastellórizon SME 1014 – 36.0694 29.6833 366–381 Madrepora oculata Yellowish fine sed. Dead Zibrowius (1979)
Betw. Karpathos and 67/20 – 35.9267 27.4850 60–80 Paracyathus pulchellus Concretions of calc. Live Zibrowius (1979)
Rhodes algae
S of Thasos SME 1587 – 40.5770 24.5870 60–70 Paracyathus pulchellus Muddy sand with Live Zibrowius (1979)
some blocs
W of Thira SME 775 – 36.3722 25.3556 73 Paracyathus pulchellus Coralligène Live Zibrowius (1979)
Betw. Euboea and SME 795 – 38.1583 24.6153 90 Paracyathus pulchellus Muddy coarse gravel, Live Zibrowius (1979)
Andros calc. algae
E of Lindos, Rhodes SME 1012 – 36.0811 28.1167 92 Paracyathus pulchellus Sandy and gravely Live Zibrowius (1979)
mud, calc. algae
S of Syros SME 816 – 37.3042 24.8667 100 Paracyathus pulchellus Coralligène, partly Live Zibrowius (1979)
dead
S of Syros SME 815 – 37.2944 24.8639 104 Paracyathus pulchellus Coralligène Dead Zibrowius (1979)
Betw. Alonnisos and SME 1547 – 39.2778 24.0306 108–112 Paracyathus pulchellus Coralligène de Live Zibrowius (1979)
Kira Panagia plateau
Betw. Euboea and SME 794 – 38.1611 24.7833 110 Paracyathus pulchellus Muddy sand with Live Zibrowius (1979)
Andros coarse clasts, calc.
algae
NW of Thirasia 67/32 – 36.5383 25.2967 110–128 Paracyathus pulchellus Clay and concretions Live Zibrowius (1979)
of calc. Algae
Johnston Bank SME 1640 – 39.3033 25.3914 120–150 Paracyathus pulchellus Muddy sand Live Zibrowius (1979)
SW of Antipsara SME 801 – 38.5167 25.5167 120–130 Paracyathus pulchellus Muddy organic gravel Live Zibrowius (1979)
SW of Thira SME 774 – 36.3528 25.3292 128–146 Paracyathus pulchellus Gravel of calc. algae Live Zibrowius (1979)
Betw. Euboea and SME 791 – 37.9194 24.6139 148 Paracyathus pulchellus Sandy-muddy detritic Live Zibrowius (1979)
Andros sed.
SE of Kastellórizon SME 1020 – 36.1070 29.5510 421 Paracyathus pulchellus Yellowish to greyish Dead Zibrowius (1979)
fine sed.
S of Thira SME 758 – 36.2958 25.3847 265–284 Paracyathus pulchellus Grey mud with Dead Zibrowius (1979)
volcanic fragments
SW of Anticythère 64/75 – 35.7000 23.3833 360 Stenocyathus vermiformis Gravely muddy sand Live Zibrowius (1979)
S of Karpathos 75/D40 – 35.0200 27.1383 600 Stenocyathus vermiformis – Live Zibrowius (1979)
SE of Kastellórizon SME 1014 – 36.0694 29.6833 366–381 Stenocyathus vermiformis Yellowish fine sed. Dead Zibrowius (1979)
Santorin – – 36.4417 25.4000 357–394 Caryophyllia calveri – Unknown Zibrowius (1980)
Hellenic trench SE of – – 35.6667 22.6500 2000–2150 Trochocyathus – Unknown Zibrowius (1980)
Kythira mediterraneus
S of Crète – – 34.5420 24.4600 2100–2500 Trochocyathus – Unknown Zibrowius (1980)
mediterraneus
Occurrences in water depths <200 m are highlighted in bold
Area: Betw. between; Gear: D dredge, T trawl, G grab; Facies: C Caryophyllia, Den Dendrophyllia, Des Desmophyllum dianthus, HG Hardground, L Lophelia, M Madrepora, N Neopycnodonte,
RB rock bottom, S: Stenocyathus, sed. sediment, calc. calcareous
91
92 J. Titschack
Table 10.2 Bathyal coral occurrences in outcrops in the region of the Aegean Sea and the adjacent Hellenic trench compiled from various sources
Latitude Longitude
Area [°N] [°E] Species Facies Reference
Crete, Phalasarna 35.5019 23.5778 Stenocyathus – Shaw et al. (2008)
vermiformis
Rhodes, Kallithea 36.3752 28.2354 Caryophyllia smithii Lindos Bay Formation Nielsen et al. (2006)
Rhodes, Kallithea 36.3752 28.2354 Lophelia pertusa Cape Arkhangelos Nielsen et al. (2006)
Formation
Rhodes, Lardos SW Hill 36.0886 28.0096 Lophelia pertusa Lindos Bay Formation Titschack et al. (2013)
Rhodes, Lardos SW Hill 36.0886 28.0096 Madrepora oculata Lindos Bay Formation Titschack et al. (2013)
Rhodes, Lindos Bay type 36.0999 28.0869 Caryophyllia smithii Lindos Bay Formation Hanken et al. (1996)
locality
Rhodes, Lindos Road Section 36.0834 28.0838 Caryophyllia sp. St. Paul’s Formation Titschack et al. (2005)
Rhodes, Lindos Road Section 36.0834 28.0838 Dendrophyllia St. Paul’s Formation Titschack et al. (2005)
cornigera
Rhodes, Lindos Road Section 36.0834 28.0838 Desmophyllum St. Paul’s Formation Titschack et al. (2005)
dianthus
Rhodes, Lindos Road Section 36.0834 28.0838 Lophelia pertusa St. Paul’s Formation Titschack et al. (2005)
Rhodes, Lindos Road Section 36.0834 28.0838 Madrepora oculata St. Paul’s Formation Titschack et al. (2005)
Rhodes, St. Paul’s Bay 36.0865 28.0889 Caryophyllia sp. St. Paul’s Formation Titschack and Freiwald (2005)
Rhodes, St. Paul’s Bay 36.0865 28.0889 Dendrophyllia St. Paul’s Formation Titschack and Freiwald (2005)
cornigera
Rhodes, St. Paul’s Bay 36.0865 28.0889 Desmophyllum St. Paul’s Formation Titschack and Freiwald (2005)
dianthus
Rhodes, St. Paul’s Bay 36.0865 28.0889 Lophelia pertusa St. Paul’s Formation Titschack and Freiwald (2005)
Rhodes, St. Paul’s Bay 36.0865 28.0889 Madrepora oculata St. Paul’s Formation Titschack and Freiwald (2005)
Rhodes, Tsunami Bay 36.0832 28.0897 Lophelia pertusa St. Paul’s Formation Titschack and Freiwald (2005)
Rhodes, Tsunami Bay 36.0832 28.0897 Madrepora oculata St. Paul’s Formation Titschack and Freiwald (2005)
Rhodes, Vasfi 36.4018 28.2214 Lophelia pertusa Lindos Bay Formation Moissette and Spjeldnæs (1995)
Rhodes, Vlycha Bay 36.1098 28.0641 Lophelia pertusa Lindos Bay Formation Kuhn (1998)
2011) where the corals occur on steep escarpments and topo- Three older ages of L. pertusa fragments from outcrops on
graphic highs (Taviani et al. 2011). While J. cailleti, S. fissilis the island of Rhodes date back to the Middle Pleistocene
and T. mediterraneus seem to be restricted to this region, L. (690–760 ka; Titschack et al. 2013) and point to the fact that
pertusa and M. oculata are also once and D. cornigera, D. L. pertusa and M. oculata were already earlier present in
dianthus and C. calveri frequently reported from the Aegean this region. Coral ages since the last glacial maximum show
Sea (Fig. 10.1a; Zibrowius 1979; Vafidis et al. 1997). a pronounced age gap between 4.5 and 10.8 ka, which
Caryophyllia smithii, G. annulata and P. pulchellus are more roughly coincide with the sapropel S1 formation in the deep
or less randomly distributed over the entire Aegean Sea when eastern Mediterranean Sea (see Vertino et al., this volume).
their shallow-water occurrences are included (Fig. 10.1). This temporal pattern is consistent with the observations by
Most reports of the coral-associated facies refer to coarse Fink et al. (2012) who suggested a temporary extinction of
grained deposits, including coral rubble and (muddy) gravel L. pertusa and M. oculata within the Santa Maria di Leuca
deposits, and hard substrates, such as hardgrounds and coral- coral province (Apulian margin, northern Ionian Sea, 500–
ligenous deposits (Zibrowius 1979). 900 m water depth) most likely due to a strongly reduced
The knowledge about the temporal occurrence of bathyal bottom water oxygen concentration, which was linked to the
corals is restricted to the Hellenic trench and Hellenic arc sapropel S1 formation. A similar control might also be sug-
islands (Fig. 10.1b). Only 21 230Th/U and 14C dates exist to gested for the bathyal corals along the Hellenic trench.
date and were obtained from the species D. dianthus (n = 6), However, the current database is by far too limited to draw
S. vermiformis (n = 5), L. pertusa (n = 4), M. oculata (n = 4), any conclusion with certainty.
C. calveri (n = 1) and C. smithii (n = 1) (paired 230Th/U – Fossil scleractinian occurrences are described from vari-
AMS14C dates obtained from one coral specimen presented ous Greek islands along the Hellenic Arc. In particular, shal-
in McCulloch et al. (2010) are counted as one date; low corals are frequently mentioned (especially Cladocora
Fig. 10.1b; McCulloch et al. 2010; Shaw et al. 2010; caespitosa (Linnaeus 1767) in: Pirazzoli et al. 2004; Kershaw
Taviani et al. 2011; Titschack et al. 2013). The available et al. 2005; Cooper et al. 2007; Titschack et al. 2008; Drinia
dates of offshore-collected corals and corals collected on et al. 2010; Mastronuzzi et al. 2014) while fossil remains of
Crete show ages ranging from 0.6 to 23.4 ka (Fig. 10.1b). bathyal corals represent a rarity and are solely described
10 Bathyal Corals in the Aegean Sea and the Hellenic Trench 93
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Taviani M, Vertino A, López-Correa M, et al (2011) Pleistocene to sity of Mediterranean deep-sea corals and cold-water corals
recent scleractinian deep-water corals and coral facies in the Eastern Chimienti G, Bo M, Taviani M, et al (this volume) Occurrence and bio-
Mediterranean. Facies 57:579–603 geography of Mediterranean cold-water corals
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Pleistocene bathyal coral communities from Rhodes, Greece. In: bution of Mediterranean cold-water corals
Mediterranean Cold-Water Corals
as Paleoclimate Archives 11
Paolo Montagna and Marco Taviani
Abstract hand, these biologically-induced geochemical signals can

Scleractinian cold-water corals preserve in their aragonite be used to investigate the processes controlling coral
skeleton information on the past changes of the physico- biomineralisation and better understand the resilience of
chemical properties of the seawater in which they grew. cold-water corals to environmental and climate changes.
Such information is stored as geochemical signals, such In the recent years, Mediterranean cold-water corals
as changes in trace elements concentration (B/Ca, Li/Mg, have been targeted for geochemically-oriented studies
P/Ca, Sr/Ca, Ba/Ca, U/Ca) or stable and radiogenic iso- and their trace elements and isotopes composition has
topes composition (δ11B, δ13C, δ18O, 14C, εNd), that are contributed significantly to developing and understanding
usually converted into environmental parameters using new and established coral proxies. Living in an environ-
empirical calibration equations. The aragonite skeleton of ment characterised by relatively warm seawater tempera-
cold-water corals is sufficiently uranium-rich to be suit- tures (13–14 °C) and high pH (8.1), the Mediterranean
able for U-series dating, providing precise and accurate cold-water corals provide the end-member geochemical
ages for the last 600–700 kyrs. This opens the possibility composition useful to derive empirical calibration equa-
to obtain reconstructions of key oceanographic parame- tions. In particular, the analysis of several specimens of
ters for the intermediate and deep water masses at sub- the cold-water corals species Lophelia pertusa, Madrepora
decadal scale resolution for climatically-relevant time oculata and Desmophyllum dianthus live-collected in the
windows in the past. However, part of the geochemical western, central and eastern Mediterranean Sea, has con-
signal incorporated into the coral skeleton is modulated tributed to the development of the Li/Mg thermometer,
by the physiology of the coral, which complicates the boron isotopes pH proxy and P/Ca nutrient proxy, as well
interpretation of the geochemical proxies. This “vital as a better understanding of the neodymium isotopic com-
effect” needs to be taken into account and corrected for to position of cold-water corals as a water mass tracer. A
obtain reliable reconstructions of past changes in seawa- multi-proxy approach has been recently applied to pre-
ter temperature, pH and nutrient content. On the other cisely U/Th-dated cold-water corals fragments from
coral-bearing sediment cores retrieved in the western and
central Mediterranean Sea, showing large changes in the
dynamics of the intermediate waters during the Holocene.
P. Montagna (*) Further investigations of fossil cold-water corals speci-
mens from different Mediterranean locations will open
Laboratoire des Sciences du Climat et de l’Environnement LSCE/ new perspectives on the reconstruction of past changes in
IPSL, CEA-CNRS-UVSQ, Université Paris-Saclay,
Gif-sur-Yvette, France
the physico-chemical properties of sub-surface waters
and their potential role in modifying the Mediterranean
Lamont-Doherty Earth Observatory, Columbia University,
Palisades, NY, USA
climate.
M. Taviani
Biology Department, Woods Hole Oceanographic Institution, Keywords
Woods Hole, MA, USA Geochemical proxies · Paleoclimate · Natural archives ·
Stazione Zoologica Anton Dohrn, Naples, Italy Cold-water corals · Mediterranean Sea

https://doi.org/10.1007/978-3-319-91608-8_11
96 P. Montagna and M. Taviani
11.1 Introduction In recent years, an increasing number of studies involving

new geochemical proxies such as isotopes (εNd), Δ14C,
In the Mediterranean Sea, anthropogenically-induced changes U/Th and trace elements, have targeted Mediterranean CWC
observed at the sea surface, such as the increasing temperature as paleo-archives of climate history (e.g. Montagna et al.
and acidification, propagate fast towards the intermediate and 2005, 2006; McCulloch et al. 2010; Dubois-Dauphin et al.
deep layers of the basin due to the very active Mediterranean 2017) (Fig. 11.1). In particular, the Mediterranean has been
overturning circulation. Indeed, hydrographic data going back the prime locus where to test trace and minor elemental com-
to 1950–1960 indicate increasing sub-surface temperature val- position of CWC with respect to paleoclimate (Montagna
ues for both the western and eastern Mediterranean basins et al. 2005), especially triggered by the recent accessibility
(Bethoux and Gentili 1996; Tsimplis and Baker 2000; Rixen and availability of a large coral collection and the use of
et al. 2005). Hydrographic and modelling data for the more advanced analytical instruments such as the new
Mediterranean Sea suggest that this basin is also experiencing generation of mass spectrometers and protocols established
a large increase in ocean acidification (OA) compared to the for the investigation of tropical (e.g. Sinclair et al. 1998;
other world areas (Touratier and Goyet 2011; Flecha et al. Fallon et al. 1999; Corrège 2006) and temperate (Silenzi
2015; Hassoun et al. 2015; Marcellin Yao et al. 2016; Maier et al. 2005; Montagna et al. 2007) corals. For instance, the
et al., this volume; Movilla, this volume), although uncertain- application of a laser ablation ICP-MS system to CWC was
ties still exist in the anthropogenic pH change of the pivotal in ensuring precise and fast analytical possibilities on
Mediterranean deep waters (Palmiéri et al. 2015). small samples and producing a great volume of data. Its
Understanding whether these recent observed modifica- successful use in tropical coral geochemistry (e.g. Sinclair
tions and trends in seawater temperature and carbonate chem- et al. 1998) prompted its application to Mediterranean
istry are the result of anthropogenic activities or are part of temperate zooxanthellate corals (Montagna et al. 2007).
the natural climate variability requires long-term (i.e. multi- Lastly, the availability of large collections of recent and
decadal to centennial and millennial) time series that extend subfossil CWC provided all the needed material to
beyond the relatively short instrumental period, especially for experiments. All such conspired for producing the first
seawater pH changes. Seawater temperature and salinity data geochemical screening of trace and minor elements in
for the intermediate and deep waters in the Mediterranean modern and late Pleistocene Desmophyllum dianthus corals
Sea are restricted to the last ~60–70 years (e.g. Painter and from the central Mediterranean Sea (Montagna et al. 2005).
Tsimplis 2003) and are very discontinuous in time and space, This set the pace for all subsequent studies on Mediterranean
limiting their use in deriving long-term changes in the past. CWC using both trace elements, stable and radiogenic
Moreover, only few continuous and relatively long (~20– isotopes (Montagna et al. 2006, 2008a, b, 2010, 2014; López
30 years) time series of thermohaline properties exist in this Correa et al. 2010; McCulloch et al. 2010, 2012b; Dubois-
basin (see Schroeder et al. 2013 and references therein). The Dauphin et al. 2017). The paleoclimate-oriented geochemical
scarcity of historical data is even more critical for the seawa- research on CWC is in full development and still is a frontier
ter carbonate system (e.g. pH, alkalinity, dissolved inorganic discipline, with applications using specimens from the
carbon), with the first high-quality measurements being con- Atlantic, Indian, Pacific and Southern oceans (see Robinson
ducted at the beginning of the 2000s (e.g. M51/2 cruise in et al. 2014 and references therein). Overall, investigation of
2001 on board R/V Meteor; Schneider et al. 2007). geochemical signals in CWC can provide a rare opportunity
The existing historical datasets are then too short to accu- to put recent anthropogenically-driven changes of key
rately attribute climate trends to natural or anthropogenic seawater parameters (e.g. T, carbonate chemistry, nutrient
processes. Consequently, the only way to extend the content) into the context of the natural variability.
instrumental record back in time is by using proxy-based Scope of this chapter is to overview the many facets
reconstructions. Intermediate and deep water physico- linked to the geochemistry of Mediterranean CWC for
chemical properties can be documented from the paleoclimate- and biomineralisation-oriented studies,
geochemistry of CWC that has been proved useful to provide discussing achievements, flaws and promising developments.
paleoclimate reconstructions at centennial to decadal-scale This chapter will not address recent studies on the prolif-
resolution (Adkins et al. 1998; Montagna et al. 2005; eration and demise of Mediterranean CWC in the past linked
Robinson et al. 2014). Pioneer geochemical contributions to specific environmental conditions, such as changes in sea-
mainly focused on coupled U/Th and 14C measurements of water temperature, oxygen content, carbonate chemistry,
the aragonite skeleton of cold-water corals (CWC) to inves- nutrient content or sedimentation regime (Malinverno et al.
tigate ocean ventilation (Adkins et al. 1998; Mangini et al. 2010; Margreth et al. 2011; McCulloch et al. 2010; Taviani
1998) as well as oxygen and carbon isotopes and trace ele- et al. 2011; Fink et al. 2012, 2013, 2015), as these long-term
ments for water mass temperature reconstructions or biomin- coral population dynamics based on geochronological data
eralisation studies (Emiliani et al. 1978; Smith et al. 2000; are discussed in other chapters of the book (see Vertino et al.,
Adkins et al. 2003; Rollion-Bard et al. 2003; Montagna et al. this volume; Wienberg, this volume; Vertino and Corselli,
2005; Shirai et al. 2005). this volume; Taviani et al., this volume).
11 Mediterranean Cold-Water Corals as Paleoclimate Archives 97
Fig. 11.1 Locations in the Mediterranean Sea where CWC were col- McCulloch et al. 2010; Taviani et al. 2011, 2016; Fink et al. 2012, 2013,
lected for geochemical analyses (U/Th and 14C dating, Nd isotopes and 2015; Montagna et al. 2014; Angeletti et al. 2015; Del Bianco et al.
Li/Mg ratios; Schröder-Ritzrau et al. 2005; Malinverno et al. 2010; 2015; Dubois-Dauphin et al. 2016, 2017; Titschack et al. 2016)
11.2 C
old-Water Corals as Paleoclimate Although highly promising, the geochemical signals con-
Archives: Environmental vs. tained in the aragonite skeleton of CWC can be difficult to
Biologically-Induced Geochemical interpret due to the presence of post-mortem alteration pro-
Signals cesses such as Fe – Mn oxide coatings and biologically-
induced modifications, commonly known as “vital effects”.
CWC are particularly attractive candidates for paleoceano- The metabolic activity of the organism partly drives the
graphic applications given they inhabit diverse environ- uptake of geochemical proxies in the coral skeleton and
ments, from the shallow-water Sub-Antarctic and Chilean obscures the primary environmental signals, complicating the
fjords to great ocean depth worldwide (Roberts et al. 2006). interpretation of climatic records. First micro-scale investiga-
CWC occur as extensive reef structures, coral carbonate tions of the CWC skeleton using micro-drilling system or
mounds, or coral patches and have a relatively large size laser ablation ICP-MS showed a strong elemental and isoto-
skeleton (from few cm to 30–40 cm) that can be sub-sampled pic heterogeneity at fine scale resolution, linked to the coral
for multiple geochemical proxies. The slow growth rate, microstructures (e.g. Rollion-Bard et al. 2003; Montagna
especially for solitary species like Desmophyllum dianthus et al. 2005; Shirai et al. 2005). The skeleton of scleractinian
(~1 mm/year; Cheng et al. 2000), allows reconstructing sub- corals is composed mainly of two structural units: centers of
decadal scale variability of intermediate water chemistry calcification (COCs) also known as centers of rapid accretion
during century-long time slices. CWC can therefore capture (CRA) or early mineralisation zones (EMZ) and the fibrous
rapid changes in the dynamics of intermediate water masses aragonite (FA) also known as thickening deposits (Stolarski
at unprecedented resolution (e.g. Eltgroth et al. 2006). This 2003; Cuif and Dauphin 2005; Nothdurft and Webb 2007;
unique possibility resides from the ability of CWC to incor- Lartaud et al., this volume). Both units are assumed to be con-
porate into their skeleton trace elements and isotopes reflect- trolled to varying degrees by the coral physiology and display
ing seawater temperature (e.g. Li/Mg), nutrient content different geochemical compositions. In particular, COCs
(P/Ca), pH and dissolved inorganic carbon (boron isotopes, show systematically lower δ18O, δ13C, δ11B and U/Ca values
B/Ca, U/Ca), ventilation age (coupled 14C and U/Th) and and higher Mg/Ca, Li/Ca, P/Ca and Ba/Ca ratios compared to
water mass tracing (Nd isotopes, εNd). Moreover, the arago- the fibrous aragonite (Montagna et al. 2005, 2008a, 2014;
nite skeleton of CWC persists in the fossil record and can be Blamart et al. 2007; Rollion-Bard and Blamart 2014). It is
radiometrically dated by U/Th, 14C, 210Pb and 226Ra tech- clear that sub-sampling different coral portions having dis-
niques (Cheng et al. 2000; Adkins et al. 2004; Frank et al. tinctive proportions of COCs vs. FA leads to different geo-
2004; Douville et al. 2010a; Sabatier et al. 2012). chemical results and eventually contrasting paleoclimate
reconstructions. Several approaches have been developed to McCulloch and co-authors provided the first Δ14C results
correct for this biological overprint (e.g. Trotter et al. 2011; from CWC collected at different water depths in the
McCulloch et al. 2012a, b; Montagna et al. 2014; see below). Mediterranean Sea, spanning the last ~20 kyrs (McCulloch
On the contrary, other coral tracers and dating methods like et al. 2010). As reported by the authors, most of the corals
Δ14C, U-series and Nd isotopes (εNd) do not suffer from Δ14C values lie on or only slightly below or above the Marine
“vital effect” and can be used to reconstruct the ventilation surface 04 curve, which is the data set published by Hughen
rate and the water mass dynamics of the intermediate/bathyal and co-authors in 2004 and used to calibrate radiocarbon
waters without performing any correction. ages for the ocean (Hughen et al. 2004). The Δ14C data of
McCulloch et al. (2010) suggest equilibrium with surface
waters and generally well ventilated intermediate and deep
11.3 Geochemistry of the Mediterranean waters in the Mediterranean Sea. The only exception is rep-
Cold-Water Corals resented by two Lophelia pertusa specimens dated at
~12.5 kyrs from the Ionian Sea with Δ14C values that fall
11.3.1 U/Th, C and Nd Isotopes
14
significantly below the marine curve (~70–80‰), likely indi-
Measurements to Constrain the Water cating conditions of water mass isolation derived from a
Mass Dynamics reduction of deep-water formation in the Adriatic Sea
(McCulloch et al. 2010). Here, the Δ14C values of 23 coral
14
C ventilation of water masses and intermediate and deep- samples reported in McCulloch et al. (2010) that cover the
water circulation rates can be evaluated from the radiocarbon last 12 kyrs have been plotted against the more recent IntCal
activity ratio (Δ14C) of CWC in the past, which reflects the 13 atmospheric and Marine 13 Δ14C curves (Reimer et al.
radiocarbon content of the seawater dissolved inorganic 2013) and converted into epsilon units (Fig. 11.2). Most of
carbon (DIC) (Adkins et al. 2002). Δ14C is calculated by the reconstructed Δ14C values of the intermediate and deep
coupling precise U/Th dating with radiocarbon measurements waters follow the atmosphere at almost constant offset and
using the formula: more than 80% of the calculated Δ14C overlap within error
with the Marine surface 13 curve. The mean epsilon value of
æ - C _ age ö
14
çe LibbyMeanLife
÷ the corals (−47.6 ± 10‰; mean ± 1σ SD) is similar to the
D14Cdeepwater = ç U / Th _ age
- 1 ÷ ´ 1000 mean difference between Marine 13 and IntCal 13 curves
ç e - TrueMeanLife ÷ (−43.1 ± 5‰; Fig. 11.2), suggesting no major changes in the
è ø
intermediate-deep water ventilation of the Mediterranean
(Adkins and Boyle 1997), where the conventional Libby Sea during the last 12 kyrs. During the sapropel S1 event
Mean Life of 14C is 8033 years and the True Mean Life is (~10.5-6 cal kyrs BP; De Lange et al. 2008), characterised by
8266 years (Stuiver and Polach 1977). This equation derives anoxic bottom water conditions and weakening or shutdown
from the definition of the measured 14C/12C ratio (see Adkins of intermediate and deep-water formation in the eastern
and Boyle 1997 for full details of the equations). The 14C Mediterranean basin (e.g. Rohling et al. 2015; Tesi et al.
content of the coral reflects both the ocean dissolved inor- 2017; Vertino et al., this volume), the Δ14C and epsilon val-
ganic carbon 14C content and the age of the coral itself. By ues of the CWC do not indicate reduced water mass circula-
correcting the radiocarbon content of the coral for the aging tion (Fig. 11.2). However, the two samples dated at ~ 7 and
component, the radiocarbon activity ratio of the water mass 9 kyrs were collected at intermediate depths in the Balearic
at the time the coral lived can be extracted. The Δ14C can Sea where ventilation conditions have not likely changed
then be compared to the contemporaneous atmosphere and during the last 12 kyrs (Dubois-Dauphin et al., 2017). In
surface global ocean Δ14C records using for example the order to track potential variations of the intermediate water
IntCal 13 and Marine 13 curves (Reimer et al. 2013) to ventilation associated to the sapropel S1 event, studies
examine rates of water mass circulation and atmosphere- should be focused on CWC collected in the central-eastern
ocean carbon exchange or 14C ventilation. The Δ14C of the Mediterranean Sea at water depths corresponding to the
corals is often express as Δ Δ14C, which is the difference Levantine Intermediate Water (LIW) or the Eastern
between the Δ14C of the sample and the Δ14C of the contem- Mediterranean Deep water (EMDW) (see for example Fink
poraneous atmosphere. However, this term does not take into et al. 2012). Moreover, reliable reconstructions of ventilation
account rapid changes in atmospheric Δ14C and a better rep- rates in the past require water mass tracers that can be used
resentation of the past ocean circulation can be achieved by to identify mixing ratio of distinct water masses, such as the
using the epsilon value (Hines et al. 2015): nutrient proxy P/Ca (Montagna et al. 2006; see below) or the
water mass provenance tracer εNd (e.g. Copard et al. 2010;
æ é D14 Csample ù ö van de Flierdt et al. 2010). A very recent study investigated
çê + 1ú ÷
e = ç ê 14 1000 ú - 1 ÷ ´ 1000 Nd isotopes in Mediterranean CWC spanning the last
ç ê D Catm ú ÷ ~13 kyrs (Dubois-Dauphin et al. 2017). Coral fragments
çê +1 ú ÷
è ë 1000 û ø were collected in the Sardinia Channel at 414 m water depth
Fig. 11.2 (a) Mediterranean

CWC Δ14C record converted
into epsilon values. Epsilon
uncertainties (1σ) are
calculated from the U/Th and
Δ14C errors. Dashed line is
the mean difference between
Marine 13 and IntCal
atmospheric 13 Δ14C curves.
(b) Mediterranean CWC Δ14C
record plotted against Marine
13 and IntCal 13 atmospheric
Δ14C curves. Error ellipses
represent 1σ correlated U/Th
and Δ14C errors (Data from
McCulloch et al. 2010). Most
of the coral Δ14C values plot
within error on the Marine 13
curve suggesting generally
well ventilated intermediate
and deep waters in the
Mediterranean Sea. The grey
shaded area indicates the
sapropel S1 interval
(~10.5-6 cal kyrs BP; De
Lange et al. 2008)
(Taviani et al. 2017) and in the Alborán Sea between 280 and limitation, there have been some attempts to use Sr/Ca as
442 m water depth (Fink et al. 2013) and analysed for Nd sub-surface water temperature proxy in CWC (e.g. Cohen
isotopes. Results reveal relatively constant εNd values et al. 2006; Raddatz et al. 2013). Cohen et al. (2006) calcu-
through time for both locations, with the sole notable excep- lated the temperature dependence of Sr/Ca ratios in a living
tion being a large shift at ~ 8.7 kyrs BP toward non-radiogenic specimen of the azooxanthellate coral Lophelia pertusa
εNd values in the Sardinian record (from −7.55 ± 0.2 at collected on the Tisler Reef in the submarine boarder
10.170 kyrs BP to −8.66 ± 0.3 at 8.703 kyrs BP), indicative between Norway and Sweden and concluded that only
of a strong reduction of the LIW formation in the eastern ~25% of the changes in Sr/Ca can be related to the tempera-
Mediterranean basin during the sapropel S1 event (Dubois- ture variation. The remaining signal is controlled by the
Dauphin et al. 2017). seasonal variation in the saturation state of the coral’s cal-
cifying fluid, which drives the skeletal “precipitation effi-
ciency”. Similarly, Raddatz et al. (2013) observed a weak
11.3.2 Cold-Water Coral Paleothermometers temperature dependence of Sr/Ca from specimens of L.
pertusa live-collected in the North Atlantic and
So far, reliable seawater temperature reconstructions using Mediterranean Sea.
the geochemistry of CWC have been difficult to achieve First attempts to use δ18O in CWC as a temperature proxy
due to the strong physiological control of the coral organ- took advantage of the large isotopic fractionation observed in
ism on the elemental uptake and isotope fractionation dur- their aragonite skeleton at fine-scale resolution to derive the
ing the skeleton formation or the impact of variables other “lines technique” method (Smith et al. 2000). Both oxygen
than temperature on traditional paleothermometers. In par- and carbon isotopes in CWC exhibit large micron-meter
ticular, temperature-sensitive proxies, such as δ18O, Mg/Ca scale variability that can only be explained by biologically-
and Sr/Ca, commonly used in annually-banded aragonite mediated vital and/or kinetic effects (e.g. Adkins et al. 2003;
tropical and temperate corals (e.g. Beck et al. 1992; Rollion-Bard et al. 2003; López Correa et al. 2010). δ18O and
Mitsuguchi et al. 1996; Montagna et al. 2007), suffer to δ13C in corals (especially CWC) show strong linear correla-
varying degrees from the effects of the organism’s physiol- tions, with the intercepts of the δ18O-δ13C trends being
ogy, which can complicate the interpretation of the geo- related with the ambient temperature (Smith et al. 2000;
chemical signal (e.g. Robinson et al. 2014). Despite this Lutringer et al. 2005). Accordingly, Smith and co-authors
developed the “lines technique” method that enables deriv- covering a large temperature range (0.8–28 °C), from warm
ing the value of δ18Ocoral − δ18Owater at apparent equilibrium shallow-water tropical environments to the cold deep-waters
(Grossman and Ku 1986), which is related to the seawater at high-latitudes. The extensive coral collection also included
temperature where the coral grew. So far, the only study that specimens of L. pertusa collected in the Adriatic Sea, Santa
applied the “lines technique” to Mediterranean CWC is the Maria di Leuca coral province and the Strait of Sicily at
one performed by López Correa et al. (2010) on two L. per- ambient temperatures of 13.65 ± 0.1 °C. By normalising
tusa specimens live-collected from the Santa Maria di Leuca Li/Ca on Mg/Ca, the resulting multi-species coral Li/Mg
coral province in the Ionian Sea. This method provided good ratios have been shown to be highly correlated with the
estimates of the ambient seawater temperature. In particular, ambient seawater temperature (r2 = 0.975), following the
using the equation of Smith et al. (2000) that accounts for the empirical exponential relationship: Li/Mg (mmol/
correction of the seawater δ18O composition, the recon- mol) = 5.41 exp (− 0.049*T) (Montagna et al. 2014)
structed temperatures (14.20 and 13.61 °C) are within (Fig. 11.3). The new Li/Mg paleothermometer does not seem
~0.3 °C of the in situ temperature value (13.9 °C). However, species-dependent and provides a precision of ±0.9 °C for
although promising in correcting for the vital effects, the the temperature reconstruction. Using Li/Mg, most of the
“lines technique” method requires a rather time-consuming biologically-mediated “vital effects” linked to Rayleigh frac-
sampling strategy at high-resolution (e.g. more than 10–15 tionation are accounted for, as both elements (Li and Mg) are
sub-samples for each coral) to obtain a single temperature likely controlled by similar uptake mechanisms and compa-
estimate and the knowledge of the past seawater δ18O com- rable biological and physico-chemical factors during coral
position. Moreover, this method is based on the assumption calcification (Montagna et al. 2014). Moreover, both ele-
that δ13Ccoral is equal to the δ13C of the seawater DIC (i.e. ments have long residence times in the ocean, on the order of
δ13Ccoral − δ13CDIC = 0‰), which is not the case since the 1–10 Ma (Lécuyer 2016), therefore the seawater Li/Ca and
carbon isotopic fractionation value between inorganic arago- Mg/Ca ratios are relatively constant through time during the
nite and bicarbonate is ~2.7‰ (Romanek et al. 1992). The late Quaternary and any changes in the metal/Ca of corals
“lines technique” method therefore presents several caveats, can be potentially attributed to variations in the environmen-
strongly limiting its use as reliable paleothermometer. tal parameters. An additional advantage of the Li/Mg method
Other efforts were focused on the application of “clumped compared to other paleothermometers stems from the fact
isotopes” (Δ47: Thiagarajan et al. 2011) and stable strontium that it requires a relatively easy analytical approach, consist-
isotopes (δ88/86Sr: Rüggeberg et al. 2008) in CWC. The ing in measuring few mg of coral material by a basic quadru-
clumped isotopes method is independent of the isotopic pole inductively coupled plasma mass spectrometry
composition of the water, thus providing unique advantages (ICP - QMS). This analytical instrument is commonly found
compared to the other proxies. However, it requires the in most geochemical laboratories and allows fast and low-
averaging of multiple replicates of homogeneous samples to cost multi-element analysis. Although few aspects of the
obtain the necessary precision (<1°C) for deep-sea tempera- Li/Mg paleothermometer still needs to be investigated, as for
ture reconstructions and recent studies suggest the presence example the precise role of coral microstructures (COCs vs.
of clumped isotope vital effects (Spooner et al. 2016). fibres) or the skeletal growth rate in modifying the geochem-
Rüggeberg et al. (2008) used stable strontium isotopes in L. ical signal (Montagna et al. 2014), this proxy is now consid-
pertusa and reported a precision of about ±1 °C and an ered one of the most promising paleothermometer for surface
apparent lack of physiological control on the fractionation and sub-surface water masses. Further development for an
of δ88/86Sr. However, subsequent studies on tropical and improved Li/Mg vs. T calibration should include the analysis
CWC based on an improved analytical method (isotope of more live-collected field coral samples and specimens
dilution TIMS vs. MC-ICP-MS) did not confirm the initial grown under temperature-controlled conditions in aquaria
δ88/86Sr vs. T positive relationship (Raddatz et al. 2013; (e.g. Orejas et al., this volume) together with a careful micro-
Fruchter et al. 2016), undermining the reliability of this geo- sampling strategy that considers the spatial distribution of
chemical proxy. COCs and fibres in the skeleton.
A very promising coral paleothermometer has been
recently developed through the analysis of the Li/Ca and
Mg/Ca composition of scleractinian corals (Montagna et al. 11.3.3 Boron Isotopes vs. Seawater pH
2009a, 2014; Case et al. 2010; Hathorne et al. 2013; Raddatz
et al. 2013). Montagna and co-authors conducted a A very active area of research in paleoceanography in the
widespread screening of the element/Ca ratios of several past decade has been the study of boron isotopes (11B and
scleractinian coral species (L. pertusa, Madrepora oculata, 10
B) in scleractinian corals for pH reconstruction (e.g.
Flabellum impensum, Porites sp. Cladocora caespitosa, Vengosh et al. 1991; Hemming and Hanson 1992; Hönisch
Acropora sp.), from live-collected and cultured specimens et al. 2004; Reynaud et al. 2004; Pagani et al. 2005; Pelejero
Fig. 11.3 Coral Li/Mg vs.

seawater temperature.
Symbols represent the Li/Mg
composition of several
tropical, temperate and CWC
spanning a temperature range
from 0.8 to 28 °C. The coral
Li/Mg ratios are inversely
correlated to the ambient
seawater temperature and
follow an exponential
relationship [Li/Mg = 5.41
exp. (−0.049 ± 0.002 × T)].
The red dots indicate the
Mediterranean CWC used for
the calibration. (Figure
modified from Montagna
et al. 2014)
et al. 2005; Douville et al. 2010b; Krief et al. 2010; studies in corals (Vengosh et al. 1991; Hemming and
Anagnostou et al. 2012; Dissard et al. 2012; Lazareth et al. Hanson 1992) and recently validated in aragonite through
2016; Stewart et al. 2016; Thil et al. 2016). Few studies have inorganic precipitation experiments (Noireaux et al. 2015).
also evaluated the boron isotopic composition of 3. It assumes that the isotopic fractionation (αB) between
Mediterranean corals, like the shallow-water species C. borate ion and boric acid is accurately determined.
caespitosa (Trotter et al. 2011) and the azooxanthellate Initially, a value of 1.0194 was obtained by Kakihana
species Caryophyllia smithii, L. pertusa and D. dianthus et al. (1977) from theoretical calculations based on
(McCulloch et al. 2012b). vibrational frequency data. More recently, experimental
The boron isotopic composition of marine carbonates, measurements in seawater gave a significantly larger
which is commonly expressed in delta notation (in per mil, value of 1.0272 (Klochko et al. 2006), which is today
‰) relative to the international standard NBS-951: widely accepted in the boron community.
d 11B = éë( 11 B /10 Bsample /11 B /10 BNBS-951 ) - 1ùû * 1000 The δ11B can be analysed in corals using different analyti-
cal techniques, including secondary ion mass spectrometry
has been shown to be a powerful tool for pH reconstruction (SIMS) (e.g. Blamart et al. 2007), positive or negative ther-
of the ocean. The boron isotope systematics in biogenic mal ionisation mass spectrometry (PTIMS, NTIMS) (e.g.
carbonates is based on the pH-dependent speciation reaction Hönisch et al. 2004; Trotter et al. 2011) and multi-collector
between borate ion [B(OH)4−] and boric acid [B(OH)3] and inductively coupled plasma mass spectrometry (MC-ICP-MS)
the different abundances of 10B and 11B in the two molecular in solution (e.g. Foster 2008; Douville et al. 2010b) or cou-
species. The δ11B-pH proxy relies on basic principles pled to a laser ablation system (e.g. Thil et al. 2016). The
(Hemming and Hanson 1992): different analytical techniques present specific advantages
and disadvantages, including sample size, time and cost of
1. The boron isotopic composition of the ocean is known analysis, matrix effects, ionisation efficiency and memory
and homogeneous. The value of 39.61‰ determined by effect that will not be discussed in the present paper (for
Foster et al. (2010) is now commonly used within the details see review by Aggarwal and You 2016).
boron community. pH is then calculated from the coral δ11B value using the
2. It assumes that only the borate ions are incorporated into following equation:
the carbonate lattice. This has been shown in initial δ11B
( ) ( )
pH = pK B - log éë d 11Bsw - d 11Bcoral / a B*d 11Bcoral - d 11Bsw + 1000* (a B - 1) ùû
where δ11Bsw and δ11Bcoral represent the δ11B in seawater and isotope theory but all the values generally lie above the borate
in the coral, respectively and pKB is the dissociation constant curve. The offset between the boron isotopic composition of
of boric acid (8.587 at 25 °C and salinity 35; Dickson 1990). the corals and the δ11B of the borate curve is explained by a
A temperature and pressure correction needs to be applied physiological control of the organism on the boron fraction-
for coral samples living in cold and deep environments, like ation (e.g. Trotter et al. 2011). This biological control seems
the CWC. to be stronger for CWC species that present higher δ11B val-
Although the theoretical foundation of the boron isotopes ues compared to tropical and temperate corals growing at
is well constrained, quantitative reconstructions of seawater similar pH conditions (McCulloch et al. 2012a). It is now
pH based on δ11B in scleractinian corals remain challenging well accepted that the δ11B of the coral reflects the pH of the
(e.g. Trotter et al. 2011). calcifying fluid (pHcf) (Trotter et al. 2011) that is actively
Figure 11.4a shows a compilation of δ11B values obtained modified by mechanisms of up-regulation controlled by the
from the aragonite skeleton of several shallow-water symbi- Ca-ATPase pump (e.g. Allemand et al. 2004). Using a large
ont-bearing coral species (white and grey symbols) and deep- suite of tropical, temperate and CWC, with few key corals
water species (coloured symbols). Overall, the δ11B values collected in the Mediterranean Sea, Trotter et al. (2011) and
decrease with decreasing seawater pH following the boron McCulloch et al. (2012a,b) developed a method to calculate
Fig. 11.4 (a) Coral δ11B vs.

seawater pH plotted with the
δ11B composition of the
borate species as a function of
seawater pH, assuming an
isotopic fractionation between
the boric acid and borate ion
of 1.0272 (Klochko et al.
2006), T = 25 °C,
salinity = 35 and depth = 5 m.
Coloured and grey symbols
represent CWC and tropical
corals, respectively. CWC
δ11B values are systematically
higher than those of tropical
corals, suggesting greater pH
up-regulation of the calcifying
fluid. (b) ΔpH (pHcf – pHsw)
vs. seawater pH. (Figure
modified from McCulloch
et al. 2012b)
the offsets in the pHcf relative to ambient seawater pH 11.3.4 Coral P/Ca as a Seawater Nutrient Proxy
(ΔpH = pHcf − pHsw) (Fig. 11.4b). These offsets are linearly
related to the ambient seawater pH with slopes varying The reconstruction of seawater nutrient concentration in
between ~−0.5 and −0.7 depending on the species, meaning the past is critical to estimate changes in productivity and
that pH changes in the calcifying space are approximately remineralisation patterns, nutrient inventory and water
one-half of those in ambient seawater. This finding has a mass mixing and eventually the contribution of the bio-
series of implications, including the possibility of using the logical pump to the levels of atmospheric CO2. The search
boron isotopic composition of the coral skeleton as a probe for a reliable nutrient proxy has been a major goal in pale-
into the processes controlling biomineralisation. Specifically, oceanography and attempts have been mainly focused on
δ11B values can be used to quantify pH up-regulation mecha- the development of geochemical tracers that can provide
nisms for different coral species, eventually providing unique information on the relative degree of nutrient utilisation in
information on the resilience of corals to ocean acidification surface waters, including for example δ13C, δ15N and δ30Si
(McCulloch et al. 2012a). The higher δ11B-derived internal (e.g. Sarnthein et al. 1988; De La Rocha 2003; Sherwood
pH of the CWC compared to the tropical corals (i.e. higher et al. 2011). Cd/Ca ratio in foraminifera and corals has
ΔpH) can be explained by the requirement of corals living to been suggested to serve as a tracer for seawater phosphate
challenging low temperature environment to sustain calcifica- (PO4) concentration, one of the main bio-limiting macro-
tion (McCulloch et al. 2012a). nutrients (Shen et al. 1987; Adkins et al. 1998; Boyle
Combining δ11B with coral B/Ca ratios as a proxy for the 1998). However, this proxy relies on the assumption that
relative abundance of borate and carbonate ions in solution modern Cd/PO4 relationship has remained the same as in
(Holcomb et al. 2016), the full carbonate chemistry of the the past oceans, which is difficult to assess. Moreover,
site of calcification can be reconstructed, notably pH, DIC recent seawater Cd/Ca values obtained within the
and aragonite saturation state. The quantification of these GEOTRACES program indicate different Cd/PO4 relation-
parameters is critical to understand the mechanisms used by ships for different ocean basins and depths (Xie et al.
the coral to promote calcification. 2015), limiting the simple use of Cd/Ca ratio as a PO4
To date, only few attempts have been conducted to recon- tracer. So far, the only direct proxy yielding absolute phos-
struct intermediate-depth water pH using the boron isotopic phate concentration is the P/Ca ratio incorporated into the
composition of CWC (e.g. Gonzalez et al. 2012) due to the coral skeleton of scleractinian shallow- and deep-water
lack of proper species-specific calibrations. Such δ11B vs. pH corals (Montagna et al. 2006; LaVigne et al. 2010;
calibrations can be empirically derived through the analysis Anagnostou et al. 2011; Godinot et al. 2011). A linear rela-
of boron isotopes from in situ live-collected specimens tionship between coral P/Ca and seawater dissolved inor-
whose ambient seawater pH has been determined and/or ganic phosphorus (DIP) has been found through the
from corals cultured at controlled pH conditions. However, analysis of the aragonite skeleton of several scleractinian
reliable pH data for intermediate-deep waters are often not specimens living and cultured under different nutrient
available or are based on pH database whose accuracy may regimes. These studies produced the first calibrations and
be uncertain. First calibrations for CWC have been obtained the first paleo-phosphorus reconstructions. In particular,
through the δ11B analysis of live D. dianthus specimens Montagna and co-authors (2006) measured P/Ca in the
retrieved from the warm and high pH Mediterranean Sea and septa of the CWC D. dianthus live-collected from the
the colder and low pH regions of the North Atlantic, Pacific Mediterranean Sea, the Australian sector of the western
and Southern Ocean (Anagnostou et al. 2012; McCulloch Pacific Ocean and the Chilean fjords (Fig. 11.5). The P/Ca
et al. 2012b). Living at relatively high pH conditions, vs. DIP calibration was then used to quantify past changes
Mediterranean CWC serve as an end- member group for of seawater PO4 concentration in the Mediterranean Sea
well-constrained empirical calibrations that can be used to (Montagna et al. 2006). However, the same authors also
extend pH reconstruction of sub-surface waters beyond the identified coral portions with anomalously high P/Ca ratios
instrumental period. related to high Mn/Ca values that suggest the presence of
In the future, efforts should be made to improve coral sam- contamination. Further studies on the phosphorus specia-
pling methods for δ11B by selecting specific micro-scale skel- tion in inorganic and coral aragonite revealed small quanti-
etal portions through micro-drilling sampling or laser ablation ties of hydroxylapatite inclusions (Mason et al. 2011),
ICP-MS as recently reported by Stewart et al. (2016). This which could potentially complicate the P/Ca interpreta-
would generate improved calibrations and more reliable sea- tion. These high-P inclusions or any additional crystalline
water pH reconstructions. Alternatively, bulk δ11B values can phases can be carefully avoided following an improved
be corrected for “vital effects” through a combination of ele- micro-sampling strategy that targets only the fibrous ara-
ments or isotopes (e.g. δ18O and δ13C) that act as tracers to gonite portions along the cross-section of the D. dianthus
quantify the biological component, following the example septum (Fig. 11.5b, c) (Montagna et al. 2009b). Compared
reported in Gonzalez et al. (2012) and Martin et al. (2016). to the centres of calcification or the outer septal surface
Fig. 11.5 P/Ca ratio

measured in the CWC D.
dianthus vs. seawater
Dissolved Inorganic
Phosphorus (DIP)
concentration. Coral P/Ca is
linearly correlated to DIP,
providing a tool to reconstruct
past changes of seawater
phosphate. The analyses were
conducted by laser ablation
ICP-MS along the fibrous
aragonite of the outer septal
surface (a). Also shown the
cross section of the septum
(b), which is formed by
fibrous aragonite and centres
of calcification (c). (Figure
modified from Montagna
et al. 2006)
(Fig. 11.5a), the internal fibrous aragonite shows lower biological overprint affects some of the climate-related
and less variable P/Ca values, yielding more accurate geochemical tracers and complicates their interpretation. A
paleo-environmental reconstructions. great effort has been made to correct for those biologically-
induced modifications and obtain reliable coral proxies but
our knowledge on the biomineralisation processes and geo-
11.4 Conclusions and Future Perspectives chemical signal incorporation is still limited.
Further investigations should be carried out to refine
CWC are emerging as an important archive of environmental existing coral paleo-proxies through a better understanding
change, providing a wealth of new information on the of their limitations related to the coral physiology in order to
chemical and physical history of intermediate-deep waters fully exploit CWC as reliable archives of oceanic variability.
that are not available from other archives. The aragonite This can be achieved by tightly coupling biology and
skeleton of CWC can be precisely dated by U/Th, 14C, 210Pb geochemistry in an integrated view of the biomineralisation
and 226Ra techniques and incorporates geochemical proxies processes. For example, following Holcomb et al. (2014),
that reflect past environmental changes. The last two decades studies should combine pH micro-sensors or pH-sensitive
have witnessed an increasing number of studies dealing with dyes with coral skeleton δ11B and B/Ca measurements in
the geochemistry of CWC, in particular the investigation of CWC cultured under controlled pCO2 conditions (Orejas
trace elements (B/Ca, Li/Mg, P/Ca, Sr/Ca, Ba/Ca, U/Ca), et al., this volume). This unique combination can provide
stable (δ11B, δ13C, δ18O), radioactive (14C, 238U) and critical information on the pH up-regulation mechanisms of
radiogenic (εNd) isotopes as proxies for seawater different coral species and on the δ11B and B/Ca proxies.
temperature, pH, carbonate ions concentration, nutrient The influence of the “vital effects” or the micro-structures
content, ventilation and water mass dynamics. These studies on the coral geochemistry can be quantified using newly-
have brought unprecedented information on environmental developed nano-micro-sampling capabilities, such as
changes of the sub-surface waters at decadal to centennial- NanoSIMS, synchrotron-based X-ray fluorescence or femto
scale resolution (e.g. Adkins et al. 1998). In addition, coral laser ICP-MS. Those analytical techniques can be used to
fragments from coral-bearing sediment cores are particularly either map fine-scale geochemical heterogeneities or selec-
attractive archives, providing centennial-millennial records tively target specific coral micro-portions showing minimal
at near continuous sub-decadal resolution for the modern biological overprint (e.g. fibrous aragonite) for proxy cali-
period and equivalent time windows into the LGM, brations or paleoclimate reconstructions.
deglaciation and Holocene. Further improvements should also be made in under-
However, one issue that is not fully resolved is the role of standing the nature of the skeletal banding in CWC and their
the coral physiology in controlling the geochemical signal growth rates, a necessary requirement to obtain accurate
and potentially biasing the paleoenvironmental multi-annual to decadal scale time-series (see Lartaud et al.,
reconstructions. Commonly known as “vital effect”, the this volume).
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96. https://doi.org/10.1002/dep2.14
Drop Chapter
Tomography of Cold-Water 12
Corals-Bearing Cores
Lorenzo Angeletti, Matteo Bettuzzi, and Maria Pia Morigi
Abstract sawing is done at a frozen status, later de-freezing may, how-

X-ray Computed Tomography is a non-destructive tech- ever, compromise fine sedimentary structures, whilst non-
nique to resolve internal structures and their three- frozen cores may suffer by disturbance due to dragging large
dimensional visualisation. Computed Tomography objects by the wire, such as coral fragments. The application
presents a wide spectrum of application in earth sciences of the non-destructive X-ray analysis is useful to document
and proves useful to unravel the architecture of sedimen- cores prior of splitting and provides a two-dimensional low-
tary cores, including those containing cold-water corals. resolution image (e.g., Foubert et al. 2007). Being sensitive
In particular the application of Computed Tomography to the water content, this analysis may at times show a satu-
not only discloses the presence of corals in the core and rated signal that masks sedimentary features. In the case of
facilitates taxonomic identification up to species-level, cores embedding CWC, the images are often oversaturated
but elucidates also their three-dimensional distribution veiling the real distribution of the coral remains (Fig. 12.1).
and taphonomic aspects. The advantages offered by Another pitfall is that taxonomic identification on X-ray
Computed Tomography-scan are continuously growing images is very difficult, so that the major value of X-ray
and is becoming a standard method of analysis for cold- analysis is the assessment of CWC presence or absence. This
water coral-bearing cores studies. “drop chapter” summarises CT-scan use to CWC-bearing
cores and presents some new results of their application to
Keywords Madrepora-mound off Linosa Island.
Computed Tomography · Cold-water corals · Madrepora-
mounds · Cores · Mediterranean Sea
Computed Tomography (CT)
Originally developed for medical diagnosis, CT application

Introduction soon expanded to a varieties of disciplines, from archaeology
(e.g., Applbaum and Applbaum 2005; Stelzner et al. 2010) to
X-ray Computed Tomography (CT) represents a quick, non- earth sciences (e.g., Petrovic et al. 1982; Holler and Kögler
destructive and routinary method in the three-dimensional 1990; Boespflug et al. 1995; Orsi and Anderson 1999;
analysis of cold-water corals (CWC) and associated macro- Cnudde and Boone 2013; Nabawy and David 2016).
fauna inside sedimentary cores. It is also functional in assess- Regarding marine research, CT analysis is a relatively quick
ing physical characteristics of the sedimentary matrix (e.g., and efficient way for non-destructive and high-resolution
density, porosity). Standard methods to analyse CWCs in identification of internal structures of sediment cores before
cores contemplate their cutting by sawing and then splitting splitting (Ashi 1997, Iturrino et al. 2004; Tanaka and Nakano
using a wire, followed by the study of resulting halves. If 2009; Tanaka et al. 2011). This includes the recognition and
analysis of CWCs inside cores (e.g., Rüggeberg et al. 2005;
L. Angeletti (*) López-Correa et al. 2007; Titschack et al. 2009, 2015, 2016;
Institute of Marine Sciences (ISMAR-CNR), Bologna, Italy van der Land et al. 2010, 2011; Douarin et al. 2014; Eisele
e-mail: [email protected] et al. 2014; Victorero et al. 2016).
M. Bettuzzi · M. P. Morigi In particular, the density contrast between CWCs and the
DIFA – Department of Physics and Astronomy, University of sedimentary matrix (i.e., mud, sand) allows reconstructing
Bologna, Bologna, Italy

https://doi.org/10.1007/978-3-319-91608-8_12
110 L. Angeletti et al.
Fig. 12.2 3-D reconstruction from Computed Tomography along core

Decors 27. It is clearly identifiable the coral (c) Madrepora oculata on
the down right side and the bivalve (b) Asperarca nodulosa. Scale
bar = 1 cm (© ISMAR-CNR Bologna)
et al. 2014). However, density measures obtained from CT

have some limitations and, in general, tend to overestimate
the density values with respect to wet bulk sediment (e.g.,
Tanaka et al. 2011; Titschack et al. 2015). Densities are
sensitive to variations in the total content of the higher
density material (coral skeletons), highlighting the proportion
of fossil clasts versus matrix and a quick estimate of the
fossil content prior core splitting (Douarin et al. 2014;
Wienberg and Titschack 2017; and Fig. 12.3).
Another advantage offered by CT scanning is that its res-
olution is often good enough to allow taxonomic identifica-
tion (even a low taxonomic level) before core opening
(Fig. 12.2).
In addition, the technique of micro-CT scanning (Ritman
2004; Lenoir et al. 2007; Schönberg and Shields 2008) is
now also applied to CWC studies and other marine carbonates
from Northern Europe and the Mediterranean but is not
discussed in this study (e.g., Beuck et al. 2007; Pirlet et al.
2010, 2012; Baum and Titschack 2016; Färber et al. 2016).
Fig. 12.1 Photograph, X-ray and Computed Tomography images from
Decors 27 core from Strait of Sicily (© ISMAR-CNR Bologna)
CT of Mediterranean Cold-Water Corals
their internal three-dimensional organisation, and is
functional to decipher taphonomic aspects (Figs. 12.1 and Only a few papers discuss CWC-rich cores also including a
12.2). CT imaging offers the possibility to estimate the CT analysis. These refer to the Roest, Traena and Stjernsund
amount of corals in cores providing also information on their reefs off Norway (Titschack et al. 2015), the Mingulay reef
volume, the ratio with respect to matrix and some size (Douarin et al. 2014), the Propeller (Rüggeberg et al. 2005),
parameters of coral fragments (e.g., Titschack et al. 2015, Challenger (Foubert and Henriet 2009; Titschack et al. 2009)
2016). CT should provide a good approximation of the bulk and Darwin Mound (Victorero et al. 2016), the Rockall Bank
density of the whole CWC-core with respect to other non- (van der Land et al. 2010, 2011) and the Banda Mound
destructive analysis (e.g., MultiSensor Core Logger: Douarin Province (Eisele et al. 2014) in the Atlantic, and, for the
12 Tomography of Cold-Water Corals-Bearing Cores 111
Fig. 12.3 Estimation of the

ratio between mud and
carbonate in the core. A
threshold segmentation value
of 2842/65535 grayvalue has
been applied to each slice.
The graph on the left
represents the volume ratio
between skeletonised particles
(e.g., corals and shells) and
the matrix (© ISMAR-CNR
Bologna)
Mediterranean from the Melilla Coral Province, Urania Bank dominated mounds off Linosa Island (Strait of Sicily) at ca.
and Santa Maria di Leuca coral Province (Titschack et al. 350 m water depth. CT was performed at the Physics
2016). Department of the University of Bologna, using laboratory
Some CWC cores from Atlantic coral mounds have been instruments designed to investigate archaeological,
analysed by means of CT-scans showing their usefulness in geological and historical objects. The Decors 27 and 30
coral quantification (Foubert and Henriet 2009; Douarin cores have been scanned with a wide field of view system,
et al. 2014; Titschack et al. 2015, 2016). CT has been proven designed for big objects. The CT system is equipped with an
to be useful in facies analysis and sedimentological X-ray tube of maximum 200 kV and 7 mA with higher
descriptions, allowing the identification of layers and laminae penetration capability with respect to a typical medical
in fine sediments, bioturbation and other sedimentary CT. The detector is a CCD camera coupled with a
structures (e.g., Rüggeberg et al. 2005; van der Land et al. photographic lens to a 45 × 45 cm2 wide scintillating screen
2010; Titschack et al. 2016). CT imaging coupled with of Cesium Iodide. The resolution achievable with such a
micro-CT scans allows the identification of early diagenetic detector is about 0.3 mm with the full field of view or
processes (different stages of dissolution, moulds formation, 0.15 mm with the half field of view, which has been used for
porosity increasing, etc.) affecting corals (e.g., Pirlet et al. our samples. That permitted to obtain a higher resolution
2010, 2012). Furthermore, sedimentary, petrographic and level compared to conventional medical CTs. Moreover, the
diagenetic analyses on CWC-bearing cores have been specific adjustment of the scanning parameters like voltage,
successfully conducted using CT-scan images (e.g., van der current, filtration and exposure time, without any dose
Land et al. 2011; Titschack et al. 2016). CT-scans permit, constraints, as is required in the very strict scanning protocols
also, taxonomic identification of skeletal parts (i.a., corals, of medical systems, allows to increase the image quality in
molluscs, bryozoans) and allow to measure relative value of terms of signal to noise ratio, increasing the global contrast,
density of the matrix sediment (e.g., Eisele et al. 2014). in addition to a higher spatial resolution with respect to a
Finally, as showed by Titschack et al. (2016) for the CWC- typical medical system. CT-scan image have been
bearing cores from the Mediterranean Sea, CT-scans allow demonstrated helpful in coral-rich layer detection, clasts size
coral skeletons (bioclasts) volume quantification, their measuring (coral skeletons) and their own orientation.
orientation and preservation patterns permitting to optimising However, standard methods, in CWC-rich core analysis,
sampling procedures for dating and identifying depositional contemplate splitting of frost or non-frost cores, although
units. Moreover, CT-scans have been proven to be a useful both present some pitfalls. Typical cutting operations have
tool to disclose aggradation rates and carbonate accumulation no effect on sedimentary features, but commonly drag corals,
rate of the CWCs (Titschack et al. 2016). A Mediterranean or other particles, along the core. On the other hand, freezing
case-study is described here based upon two CWC-bearing is useful to prevent the displacement of skeletonised particles,
cores (Decors 27 and 30, 214 and 150 cm long, respectively: but water frost-defrost generally alters or masks fine-scale
Fig. 12.1) collected from dead and unburied Madrepora- structures.
Conclusions Färber C, Titschack J, Schönberg CHL, et al (2016) Long-term macro-

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Acknowledgements Captain, crew and shipboard staff of R/V Urania
López-Correa M, Freiwald A, Demuth M (2007) Cold-water corals
cruise Decors are thanked for their efficient and skilful cooperation at
as climate archives in the ocean depths. Computer tomography
sea. Marco Taviani and Paolo Montagna provided helpful comments to
of sediment cores provides outstanding insights for geologists.
earlier versions of this manuscript. We acknowledge Jurgen Titschack,
SOMATOM Sess 21:52–54
Andrés Rüggeberg and Cova Orejas for their useful reviews that helped
Nabawy BS, David C (2016) X-ray CT scanning imaging for the Nubia
improving the clarity of the text. This paper is Ismar-Bologna scientific
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Drop Chapter
Changing Views About Mediterranean 13
Cold-Water Corals
Marco Taviani
Abstract
provinces and other occurrences known especially in the
Sedimentary deposits in southern Italy are renowned since
central and western basins (Taviani et al. 2017). However,
the nineteenth century for their important legacy of deep-
for long and well up a decade ago or so, this biological situ-
water benthic invertebrates, comprehensive of cold-water
ation was circumstantially masked by the Mediterranean’s
corals, which includes a number of extant taxa of Atlantic
unusually common fossil coral legacy resulting from the
affinity. Interestingly, at the dawn of the biological explora-
basin geodynamic evolution in the Cainozoic (Taviani et al.
tion of the deep-sea and because of these fossils, it was pro-
2005a). The present text is meant to address this rather
posed that the Mediterranean was one centre of origin of
intriguing story by commenting upon an historical and a con-
deep-water benthos that later migrated into the Atlantic.
temporary situation, respectively.
More recently in time, it was postulated that the cold-water
corals fauna in the Mediterranean was in strong decline after
having being prosperous at times in the Pleistocene. The
eguenza or When Deep-Sea Forms Got
S
advent of remotely operated vehicle exploration reversed
Discovered First on Land Than Offshore
this paradigm by revealing many sites of active coral life.
The overall picture is, however, more complex since the
The Sicilian naturalist Giuseppe Seguenza was undoubtedly
Mediterranean cold-water corals indeed suffered times of
one of the most prestigious Mediterranean paleontologists of
strong demise in response to climatic reasons and still
the nineteenth century (Bonfiglio 1991). His many scientific
nowadays sectors of the basin have not fully recovered.
achievements encompassed the study of terranes in Southern
Italy, which hosted numbers of benthic deep-water inverte-
Keywords brates, especially molluscs and corals (Seguenza 1864,
Cold-water coral · Pleistocene · Recent · Mediterranean 1873–1877, 1875, 1880). At those times, the exploration of
basin · Atlantic Ocean · Historical biology · Paleontology · the deep-sea was really as its beginning and quite little was
Biogeography known about the inhabitants of Atlantic and Mediterranean
waters. Because the Pleistocene deposits of Calabria and
Sicily contain many (morphologically-based) extant taxa
(Fig. 13.1a–c), this paleontological material got in many
Introduction cases to be known to Science (and some species even estab-
lished) on fossil material almost contemporaneously when
Today the widespread presence of live cold-water corals not before being found alive in the Atlantic or Mediterranean
(CWC) in the Mediterranean Sea, also known as ‘white cor- waters by earlier expeditions, such as those of the Lightning,
als’, is an ascertained fact documented by a number of CWC Porcupine and Washington ships. This is especially true for
molluscs (Taviani 1976; Di Geronimo 1991) but equally
applies to scleractinian corals (Lophelia, Madrepora,
M. Taviani (*) Desmophyllum, Caryophyllia etc.) with many fossil species
introduced by Seguenza, which are now attributed to living
Biology Department, Woods Hole Oceanographic Institution, taxa (Zibrowius 1974, 1991; Vertino 2003, 2004; Vertino and
Woods Hole, MA, USA
Di Geronimo 2003). Indeed, Duncan (1870) already com-
Stazione Zoologica Anton Dohrn, Naples, Italy mented upon the situation of some CWC being collected
alive in the eastern Atlantic and either only known as fossils
https://doi.org/10.1007/978-3-319-91608-8_13
116 M. Taviani
Fig. 13.1 (a) Fossil Lophelia (as Lophohelia) from Sicily reproduced a muddy sediment, a common situation at many Mediterranean sites,
in the plate 11 of the famous monograph Disquisizioni paleontologiche bar = 5 cm (R/V Urania, Station ARCO-47, 43°10.82′ Lat. N – 15°09.10′
intorno ai Corallarii fossili delle rocce terziarie del distretto di Messina, Long. E, 233 m), (d) Lush CWC reef imaged by the ROV in the Bari
published by Giuseppe Seguenza in 1864, (b) Pleistocene limestone Canyon, showing healthy L. pertusa (right) with expanded polyps,
embedding pieces of Lophelia pertusa from the Trapani creek outcrop, bar = 10 cm (R/V MinervaUno, Station SIRIAD16-5, 43°17.65′ Lat.
next to the town of Messina, one of Seguenza’s classic localities cited in N – 17°07.94′ Long. E, 244 m). (Photographs: c, d: © ISMAR-CNR
his 1864 monograph, bar = 1 cm (photo courtesy of A. Vertino), (c) Last Bologna)
glacial subfossil cold-water corals (prevalently L. pertusa) embedded in
in Sicily or both fossil and live in the Mediterranean Sea Reversing the Paradigm
(e.g., Lophelia pertusa). This bizarre situation (fossils known
in the Mediterranean, living counterparts found in the east Coming to modern times, another paradoxical situation
Atlantic) led Giuseppe Seguenza to develop the view that regards the submarine presence of CWC in the Mediterranean
this deep-sea fauna (in his case-study molluscs) did originate Sea and a radically-changed interpretation within a few
in the Mediterranean to later spread into the adjacent Atlantic decades. Because of a persistent paucity until a few years
Ocean (Seguenza 1870). At any event, it was already identi- ago of biological investigation aimed at the Mediterranean
fied in the nineteenth century a major biogeographic point: deep-sea hard substrates, only some fragmentary CWC
the Mediterranean CWC (with abundant fossils in outcrops information was for long available to marine scientists. It
and scant records in the sea) by large compares at specific mainly derived by pioneer French submersible expeditions
level with northeastern Atlantic counterparts (Zibrowius and as by-catch products of marine geological sampling by
1980). Unwillingly and subtly, this fact possibly conspired to means of chained heavy dredges, mostly by French and
their later interpretation as animals doing better in cold Italian surveys (revised in Taviani et al. 2005a, 2011a,
waters whilst being troubled in warm situations. 2017). In the years preceding the new millennium, the situ-
13 Changing Views About Mediterranean Cold-Water Corals 117
ation was such that only a few repositories contained sub- or partial recovery in the Holocene, although not every-
stantial CWC Mediterranean material, and this was almost where (Remia and Taviani 2005; McCulloch et al. 2010;
totally represented by loose dead material (Fig. 13.1b), Fink et al. 2012, 2015; Vertino et al. 2014, this volume).
often highly degraded, up to corals embedded into authi- Thus, the vision that is kept today about CWC viability in
genic limestones (Selli 1970; Cita et al. 1979; Taviani and the Mediterranean needs necessarily to be more articulated.
Colantoni 1979, 1984; Zibrowius 1981, 1987, 1991; Taviani The Mediterranean Sea is neither a ‘Coral Cemetery’ as
et al. 2005a, 2011b, this volume). Probably, the largest of thought for a while, nor is a ‘Coral Sea’ in all its geographic
such collections was at the time hosted in the Laboratory of extension. It surely maintains many situations optimal to
Marine Geology of CNR in Bologna. The extensive 14C dat- CWC growth, but other areas are still not recovering their
ing of those specimens, combined with scattered radiocar- past prosperity, a lesson on how delicate and dynamic could
bon dates published by other scholars, demonstrated that the be the life of CWC in the Mediterranean Sea, which is now
quasi-totality of dredged corals was late Pleistocene in age threatened also by global warming, ocean acidification and
(Delibrias and Taviani 1985). Incidentally, a later confirma- anthropogenic disturbances.
tion of such ages came from the application of U-series dat-
ing (McCulloch et al. 2010). These dates supported earlier Acknowledgements I am very indebted to a number of people who
views about a dramatic CWC decline in the Mediterranean provided inspiration to work over the years on Mediterranean CWCs
and it would be impossible to name all of them but I wish to mention at
basin after having enjoyed better times in the Pleistocene least Paolo Colantoni, Helmut Zibrowius, André Freiwald, Paolo
(Blanc et al. 1959; Zibrowius 1980), and a paradigm was set Montagna, Lorenzo Angeletti, Alessandro Remia, and Agostina Vertino.
on. At the turn of the millennium, an impressive jump in the Lorenzo Angeletti kindly helped with figures and Agostina Vertino
interest for the deep-seabed, a wider use of marine technolo- provided field images of Seguenza’s sites in Sicily. Positive comments
provided by reviewers Antonietta Rosso and André Freiwald, and by
gies, and serendipitous findings in the Mediterranean co-editor Carlos Jiménez are gratefully acknowledged. This paper is
opened the doors to challenge this view. How this happens Ismar-Bologna scientific contribution n. 1937, and is part of EU F.P. VII
is known: first the discovery of the Santa Maria di Leuca Projects COCONET, (contract no. 287844), and EVER-EST (contract
(SML) lush living CWC grounds in the northern Ionian Sea no. 674907), DG Environment programme IDEM (grant agreement No
11.0661 /2017/750680/SUB/EN V.C2), and the Flag Project Ritmare
(Tursi et al. 2004; Taviani et al. 2005b) informed about the (Ricerca Italiana per il Mare) project.
persistence of Lophelia and Madrepora in the Mediterranean.
The later discovery of similar CWC grounds south of Malta
(Schembri et al. 2007; Knittweis et al., this volume) pro-
vided unquestionable evidence that SML was not a sporadic References
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DTA/06-2011, p 705 Cross References
Taviani M, Vertino A, López Correa M, et al (2011b) Pleistocene to
recent scleractinian deep-water corals and coral facies in the Eastern Chimienti G, Bo M, Taviani M, et al (this volume). Occurrence and
Mediterranean. Facies 57:579–603 biogeography of Mediterranean cold-water corals
Taviani M, Angeletti L, Canese S, et al (2017) The “Sardinian cold- Knittweis L, Evans J, Aguilar R, et al (this volume) Recent discoveries
water coral province” in the context of the Mediterranean coral eco- of extensive cold-water coral assemblages in Maltese waters
systems. Deep-Sea Res Part 2 Top Stud Oceanogr 145:61–78 Taviani M, Vertino A, Angeletti L, et al (this volume) Paleoecology of
Trincardi F, Foglini F, Verdicchio G, et al (2007) The impact of cas- Mediterranean cold-water corals
cading currents on the Bari Canyon System, SW-Adriatic Margin Vertino A, Taviani M, Corselli C (this volume) Spatio-temporal distri-
(Central Mediterranean). Mar Geol 246:208–230 bution of Mediterranean cold-water corals
Part II
Present
Taxonomy, Genetics and Biodiversity
of Mediterranean Deep-Sea Corals 14
and Cold-Water Corals
Alvaro Altuna and Angelo Poliseno

Within the Mediterranean basin there are 82 species of
deep-sea corals belonging to six orders of the phylum Corals pertain to different orders of the Phylum Cnidaria
Cnidaria (Antipatharia, Scleractinia, Zoantharia, (Table 14.1), which includes diblastic solitary or colonial
Alcyonacea, Pennatulacea and Anthoathecata), with the animals with primary radial or biradial symmetry and gross
Alcyonacea (40) and the Scleractinia (25) being the most anatomical simplicity (Hyman 1940). Although their occur-
speciose. Thirteen species have a pronounced habitat- rence in the deep-sea is known since the eighteenth century
building ability at depths >200 m. Remarkable sites charac- (Roberts et al. 2006), their diversity and functionality in the
terised by rich coral frameworks and gardens have been deep-sea environments has been only recently explored
found in biodiversity surveys during the last years, revealing thanks to the implementation of new research technologies.
that some species are more abundant than previously Given their vertical growth and due to their key-role in struc-
thought. However, in terms of species richness, the turing the deep-sea environments, many corals provide sub-
Mediterranean deep-sea coral fauna is less diverse when strate, food, shelter and nursery for other species (Rogers
compared with the nearby Atlantic areas. This discrepancy 1999; Baillon et al. 2012; De Clippele et al. 2015; Jiménez
is probably in part due to unfavourable environmental con- et al. 2016). Some species are habitat-builders able to struc-
ditions of the deep Mediterranean Sea, and to differences in ture communities that are widely distributed in European
sampling efforts between both areas. In this respect, consid- waters (Freiwald et al. 2004; Roberts et al. 2009; Mastrototaro
erable efforts have been recently done in terms of deep-sea et al. 2010; Bo et al. 2015). Once their importance was rec-
fauna inventories. Nevertheless, updates made to the ognised, the scientific literature on these animals grew rap-
Mediterranean inventory of deep-sea corals since the begin- idly from the mid-1990s onwards (see Willison et al. 2001;
ning of the twenty-first century are few except for the octo- Roberts et al. 2009; Roberts and Cairns 2014). Many studies
corals. Therefore, ten species were included to the include Mediterranean species (e.g., Zibrowius 2003; Taviani
Mediterranean inventory, among which two have been et al. 2005; Freiwald et al. 2009; Mastrototaro et al. 2010; Bo
newly described. The species concerned belong to the orders et al. 2014, 2015).
Scleractinia (1), Pennatulacea (1) and Alcyonacea (8). Three main groups of Mediterranean deep-sea corals can
be distinguished according to their ability to form habitat: (i)
Keywords those constructing frameworks on hard bottoms (white coral
Cnidaria · Cold-water corals · Mediterranean Sea · communities) capable of modeling the environment, as the
Taxonomy · Genetics · Biodiversity · Deep-sea scleractinians Lophelia pertusa and Madrepora oculata (see
Zibrowius 2003; Taviani et al. 2005; Freiwald et al. 2009;
Orejas et al. 2009; Mastrototaro et al. 2010; Gori et al. 2013);
(ii) those forming “meadows” or “gardens” on hard bottoms
A. Altuna (*) (Leiopathes glaberrima, Parantipathes larix, Viminella fla-
INSUB, San Sebastián, Spain
gellum) (see Giusti et al. 2012; Bo et al. 2014, 2015; Grinyó
et al. 2016), and soft-bottoms (Isidella elongata, see Pérès
A. Poliseno
and Picard 1964; Maynou and Cartes 2011; Cartes et al.
Department of Earth and Environmental Sciences, Palaeontology
& Geobiology, Ludwig Maximilians Universität München, 2013; Bo et al. 2015; Mastrototaro et al. 2017); and (iii)
Munich, Germany those of unequal abundance in hard and soft bottoms, that are

https://doi.org/10.1007/978-3-319-91608-8_14
122 A. Altuna and A. Poliseno
Table 14.1 Mediterranean deep-sea corals

Phylum Class Subclass Order Suborder N° sp. A
Cnidaria Anthozoa Hexacorallia Antipatharia 5 3
Scleractinia 25 4
Zoantharia Macrocnemina 1 –
Octocorallia Alcyonacea Alcyoniina* 7 –
Calcaxonia 8 3
Holaxonia 18 –
Scleraxonia* 1 –
Stolonifera* 6 –
Pennatulacea 10 2
Hydrozoa Hydroidolina Anthoathecata Filifera 1 1
Total 82 13
(A) habitat-forming species at depths >200 m
(*) Taxa for which the taxonomic status is still controversial or not fully resolved; a suborder level is unacceptable for some authors
frequently associated to the communities structured by other to refer to those corals living at certain depths (see Morgan
organisms. Some of these species are poorly known and only 2005), although some authors do not concur (e.g., Freiwald
rarely collected (see Mastrototaro et al. 2010; Bo et al. et al. 2004). Some authors consider CWCs those cold-affinity
2012a, 2014). The species in (i) and (ii) that live at certain species able to form structural habitat and commonly living
depths are few and are commonly associated to the cold deeper than 200 m depth (see Chimienti et al., this volume).
water coral (CWC) concept (see Freiwald et al. 2004; Roberts In this chapter we review the Mediterranean corals living
et al. 2006; Chimienti et al., this volume). deeper than 50 m (deep-sea corals), no matter whether they
In this contribution, we provide information on the pres- are capable of forming habitat deeper than 200 m depth. The
ent state of knowledge of Mediterranean deep-sea corals, Mediterranean deep waters are homothermic below 200–
with special emphasis placed on their biodiversity, distribu- 300 m depth, with temperatures ranging from 13 °C (western
tion, systematics and molecular taxonomy. We include a list basin) to 15.5 °C (eastern basin) (Emig and Geistdoerfer
of species with their depth ranges and bibliographic resources 2004). This can be a reason why CWCs Mediterranean fauna
for taxonomic identification. is not as rich as in nearby Atlantic areas, as CWCs are largely
restricted to temperatures between 4 °C and 12–13 °C
(Freiwald et al. 2004; Roberts et al. 2006). In our review we
14.2 S
ome General Insights into the include the coral species living in part of the circalittoral and
Anatomy and Systematics of the in the bathyal zones. The former extends from the lower limit
Deep-Sea Corals and Cold-Water Corals of occurrence of the photophilous algae to the lower limit of
the sciaphilous algae; the bathyal starts in the lower limit of
14.2.1 Cold-Water Corals? Deep-Sea Corals? growth of the multicellular algae and comprises the conti-
nental slope and the area immediately below (Pérès and
Cairns (2007) suggested a definition of coral that reads as Picard 1964). In bathymetric terms, the circalittoral extends
follows: “Corals: animals in the cnidarian classes Anthozoa in the Mediterranean Sea from ~30–40 m depth to the shelf-
and Hydrozoa that produce either calcium carbonate (arago- break at ~100–110 m, and the bathyal from this lower limit
nitic or calcitic) secretions resulting in a continuous skeleton to 3000 m (Pérès and Picard 1964; Emig and Geistdoerfer
or as numerous, usually microscopic, individual sclerites, or 2004). To our best knowledge, there are no corals living at
that have a black, horn-like, proteinaceous axis”. For this abyssal depths (>3000 m, see Laubier and Emig 1993) in the
author, deep-water corals are those living deeper than 50 m Mediterranean Sea.
(see also WWF/IUCN 2004; Ramirez-Llodra et al. 2010;
Yesson et al. 2012). This depth limit was proposed to sepa-
rate deep/cold-water from shallow-water species, and reflects 14.2.2 Anatomy and Systematics
the tendency of zooxanthellate scleractinians and octocorals
to occur in waters shallower than 50 m, unlike azooxanthel- The Mediterranean deep-sea corals and CWCs belong to the
late species which occur typically deeper (>50 m) (Cairns classes Anthozoa and Hydrozoa, and they are classified in
2007; Yesson et al. 2012). The terms deep-water corals, six orders (Table 14.1). According to the previous definition
deep-sea corals and CWCs are commonly used indistinctly of Cairns (2007), all the soft-bodied species included in the
14 Taxonomy, Genetics and Biodiversity of Mediterranean Deep-Sea Corals 123
hexacorallian orders Actiniaria, Ceriantharia and

Corallimorpharia are excluded. Additionally, the Hydrozoa
are represented by a single family (Stylasteridae). Although
several species belonging to these orders have similar exter-
nal features, differences are significant in the anatomy of the
polyps as shown in cross-section (see Häussermann et al.
2003a; Roberts et al. 2009), and by their skeletons. Cnidarian
polyps typically have a hollow central body cavity (coelen-
teron) opening by the mouth, which is surrounded by a vari-
able number of tentacles, and cnidae; the cnidome is the
entire complement of the cnidae types in a given taxon
(Bouillon et al. 2004). In the class Anthozoa, the mouth is
followed by the actinopharynx, a tube-like structure which
communicates with the gastrovascular cavity (see Roberts
et al. 2009 and references therein). Its inner edge has one
(Octocorallia) or more siphonoglyphs (Hexacorallia), which
function is to conduct water into the body cavity (Hyman
1940). This cavity is divided into compartments by complex
longitudinal structures called mesenteries (septa) that can be
paired (Scleractinia, Zoantharia) or unpaired (Antipatharia,
Octocorallia) (see Hyman 1940; Bayer et al. 1983;
Häussermann et al. 2003a and references therein). The
hydrozoan polyp lacks actinopharynx and mesenteries (see
Bouillon et al. 2004). The type and nature of skeletal struc-
tures are essential to distinguish among the different groups
of Mediterranean corals. The skeletons may be proteinaceous
(Antipatharia, Zoantharia), calcareous (Scleractinia,
Fig. 14.1 Calicular structures in scleractinians. (a) Caryophyllia inor-
Fig. 14.1), or mixed types even in a single species (many nata, calicular view showing arrangement of septa (S1–S4), columella
octocorals Fig. 14.2a). Mineralised skeleton can be continu- (c) and pali (p); Marseille, 60 m depth (specimen sent by H. Zibrowius).
ous (Scleractinia, Fig. 14.1, Stylasteridae), or discontinuous (b) Dendrophyllia cornigera, calicular view showing arrangement of
septa according to Pourtalès plan, with septa fused forming triangles
in the form of calcareous sclerites of different shapes
(pp, arrow); c, columella. The porosity of the corallum is characteristic
(Octocorallia, Fig. 14.2a–g); the sclerome is an inventory of of the Dendrophylliidae. Alborán Sea, depth unknown. Scale bar:
all sclerites occurring in a given octocoral taxon. The analy- a = 4 mm; b = 10 mm
sis of the cnidomes of the deep-sea corals is limited, although
there are ongoing studies on Mediterranean antipatharians
(Bo 2008). Roberts et al. (2009) provided an identification 14.3 T
he Mediterranean Deep-Sea Corals
key for the coral groups Antipatharia, Octocorallia, and Cold-Water Coral Groups
Scleractinia, Stylasteridae and Zoantharia based on charac-
teristics of their mesenteries, tentacles and skeletons. 14.3.1 Class Anthozoa, Subclass Hexacorallia
Discrepancy between morphological and molecular data
are extended over the phylum. The phylogenetic reconstruc- Hexacorallians are solitary or colonial anthozoans having
tions of many cnidarian taxa vary according to the morpho- mostly hexamerous symmetry and simple tentacles rarely
logical characters and molecular markers considered branched. The anatomy of their polyps is more complex and
(Fig. 14.3). However, it is interesting to notice that one of the variable than that of octocorals, with one, two or exception-
most recent phylogenetic studies of the phylum Cnidaria, ally more siphonoglyphs and generally numerous mesenter-
based on genomes and transcriptomes (Fig. 14.3d), coincides ies. Polyps do not exhibit polymorphism. The subclass
with cladistic morphological analyses (Fig. 14.3a). Molecular includes six orders, with Antipatharia, Scleractinia and
studies are revolutionising Cnidarian systematics, therefore, Zoantharia having representatives in the Mediterranean
changes in the classification as well as taxonomic revisions deep-sea coral fauna (Table 14.1). Häussermann et al.
are expected in the near future. (2003a, b) published a general overview of the anatomy of
the class Anthozoa and the subclass Hexacorallia, including
Fig. 14.2 Some morphological features of holaxonians. Gorgoniidae, the anthocodial sclerites in a collaret (co) (sclerites arranged in trans-
(a) Leptogorgia sarmentosa. Part of a colony showing horny axis (a) versal rows) and points (p) arrangement; (a), anthocodia. Murcia,
and coenenchyme (c). Alborán Sea, depth unknown; (b) Another speci- Spain, depth unknown (© National Museum of Natural Sciences,
men showing slit-like apertures from polyps (arrows), same zone; (c) Madrid, MNCN 2.04/1054). (e) Balloon-clubs from specimen c. (f)
Eunicella singularis, polyps arrangement on stem (arrows). Alborán Spindles from b. (g) Thornscale from d. Scale bar: a–c = 2 mm;
Sea, depth unknown. Plexauridae, (d) Paramuricea clavata, part of a d = 1 mm; e, f = 0.05 mm; g = 0.2 mm
branch showing polyps. Arrows show calyx with thornscales (ca), and
a detailed glossary of anatomical terms covering all orders.

a Hydrozoa b Hydrozoa Daly et al. (2003) provided a summary of the diagnostic
morphological features for each hexacorallian order.
Scyphozoa Scyphozoa
Cubozoa 14.3.1.1 Order Antipatharia

Cubozoa
The Order Antipatharia is a group of non-calcareous colonial
Anthozoa Anthozoa cnidarians comprising about 247 species included in 7 fami-
lies and 41 genera (Brugler et al. 2013). Also known as black
c d Hydrozoa
corals, antipatharians are characterised by a colony consist-
Hydrozoa
Scyphozoa ing of a proteinaceous spiny rigid axis and numerous small
Scyphozoa six-tentacled polyps often no more than a few millimeters in
Cubozoa diameter. These corals have six primary mesenteries, either
Octocorallia Cubozoa
zero, four or six secondary mesenteries, and a spiny skeletal
Hexacorallia Anthozoa
axis (Opresko 2001; Daly et al. 2007). They are important
slow-growing, frequently long-lived, habitat-forming ani-
Fig. 14.3 Overview of the phylogenetic reconstructions of Cnidaria
based on different morphological and molecular sources. (a) morpho- mals. Black corals may have different types of colonies rang-
logical cladistic analysis (Schuchert 1993); (b) phylogenetic recon- ing from unbranched whip-like to densely ramified
struction based on morphological characters, 18S rRNA and the tree-like.
mitochondrial 16S rRNA (Bridge et al. 1995); (c) molecular phylogeny
based on complete mitochondrial genomes (Kayal et al. 2013) and (d)
Antipatharians have been the subject of taxonomic diffi-
phylogenomics based on genomes and transcriptomes (Zapata et al. culties until very recent times. The historical aspects and lit-
2015) erature on the topic were reviewed by Opresko (1974) and
Brugler et al. (2013). Despite difficulties persist in some rnl). The longest IGRs seem to be those between trnW and
taxa, the systematics of these organisms was clarified mostly Nad2 (igrW) and between Nad5 and Nad1 (igrN). To date the
due to the revisions of Opresko (2001, 2002 and subsequent complete mitogenomes of only four species are available in
papers), with the families Antipathidae and Leiopathidae, the public repositories (Brugler and France 2007; Kayal
still pending. Further changes are expected in the current et al. 2013), but none of them occur in the Mediterranean
systematic scheme when their revisions will be completed. Sea.
The habitat requirements of the Antipatharia were sum- Molecular analyses including Mediterranean species are
marised by Wagner et al. (2012) and Bo and Bavestrello (this scarce. Antipathella subpinnata and Leiopathes glaberrima
volume). Most antipatharians live attached to a hard sub- have been placed, according to phylogenetic analyses, into
strate by means of a basal holdfast, but free-living colonies families Myriopathidae and Leiopathidae, respectively
occur in soft-bottoms as well. They are important compo- (Lapian et al. 2007; Bo et al. 2012b; Brugler et al. 2013).
nents of different Mediterranean CWC communities, includ- This result agrees with the morphology-based taxonomy of
ing white corals, and typically form large ‘sea forests’ these species (see Bo et al. 2008). One of the first studies
(Angeletti et al. 2014; Bo et al. 2014, 2015). performed on the Mediterranean species L. glaberrima has
surprisingly reported the presence of a COI intron (Sinniger
Taxonomy and Taxonomic Characters and Pawlowski 2009). Leiopathes glaberrima and Antipathes
The families were keyed out by Brugler et al. (2013). They dichotoma have been included in the phylogenetic recon-
are principally distinguishable by the internal and external structions by Brugler et al. (2013).
anatomy of the polyps and their size, the growth form of the
corallum, the size and shape of spines and the morphology Mediterranean Species
and characteristics of the pinnules. These characters are also The six Mediterranean species currently known belong to
important at lower levels (genus and species). The spines of four families and four genera, Antipathidae (A. dichotoma
the skeleton are usually less than 0.5 mm tall and are com- and Antipathes fragilis), Leiopathidae (L. glaberrima),
monly used to distinguish black corals from other tree-like Myriopathidae (A. subpinnata and Antipathella wollastoni),
anthozoans. Largely neglected in the literature as a taxo- and Schizopathidae (Parantipathes larix). Among these, five
nomic character, the cnidome could be a key element for spe- live at depths higher than 50 m, and one, A. wollastoni, is
cies level identification (Bo 2008). known only from a single record near the Gibraltar Strait at
We refer to Brook (1889) for a detailed description of the 35 m depth (Ocaña et al. 2007) and is therefore not consid-
anatomy of antipatharians, to Opresko et al. (2014) for a ered a deep-sea species. Three are characteristic habitat-
glossary with technical terms and morphological descrip- building species at depths higher than 200 m (CWCs) (A.
tions, and to Opresko (2001, 2002 and further papers) for dichotoma, L. glaberrima, P. larix).
taxonomic revisions with diagnoses of all families and gen- The five deep-sea antipatharians were first described in
era, and description of type material and identification keys the Mediterranean Sea, and except for A. fragilis, described
to genus level. In addition, Daly et al. (2007) and Brugler by Gravier (1918), they are known in this area since the eigh-
et al. (2013) provided diagnoses for each family, and Opresko teenth century. Apart from A. fragilis, the types or neotypes
and Försterra (2003) described the Mediterranean species. of all species have been re-described in the last years, includ-
ing SEM (Scanning Electron Microscope) images of pin-
Molecular Aspects nules and spines (see Opresko and Baron-Szabo 2001;
Phylogenetic analyses on the Order Antipatharia have been Opresko 2001, 2003). Investigations on the cnidome of most
performed using both, nuclear and mitochondrial molecular Mediterranean species have been recently undertaken (see
markers. Brugler et al. (2013) explored the evolutionary his- Table 14.2).
tory of the order using 18S and 28S rRNA, and mitochon- All Mediterranean antipatharians are hard-bottoms spe-
drial intergenic regions (IGRs). These authors reported the cies and have mostly a bushy appearance (Fig. 14.4a–c, see
presence of a novel group I intron within the COI gene, also Bo et al. 2011, 2012a). Leiopathes glaberrima is prob-
encoding for a putative homing-endonuclease, in six differ- ably the most easily distinguishable species, due to its large
ent antipatharian genera. Three families (Antipathidae, and irregularly branched corallum with colonies up to 2 m
Aphanipathidae and Cladopathidae) comprise polyphyletic high, orange polyps and a black, smooth and brilliant axis
assemblages. The Antipathidae is the most speciose family, with minute spines (Fig. 14.4c, see a redescription of the
although it has been clearly defined as a taxonomic “dump- type in Opresko and Baron-Szabo 2001). Parantipathes larix
ing” ground due to its polyphyletic origin (Daly et al. 2007). is rather different, as it has monopodial to sparsely branched
Concerning the mitochondrial genome of black corals, bottle-brush colonies up to 2 m in height and frequently pur-
this has a size ranging from 17,000 to 20,000 bp with 14 pro- ple in colour (Fig. 14.4d, see also Bo et al. 2014). Stem and
tein coding genes and two ribosomal RNA subunits (rns and branches are pinnulate, with six rows of simple pinnules on
Table 14.2 Deep-water corals (depth >50 m) known from the Mediterranean Sea
Species A B C D E F Remarks Species reference
Class Anthozoa
Subclass Hexacorallia
Order Antipatharia
Family Antipathidae
Antipathes dichotoma c h 90–645 x x Cnidome described by Bo et al. (2011), Opresko (2003) and Bo et al.
Pallas, 1766 who summarised Mediterranean records (2011)
including a distribution map
Antipathes fragilis Gravier, c h 70–600 x Last new antipatharian first described from Gravier (1918)
1918 the Mediterranean Sea, and last one added
to the inventory
Family Leiopathidae
Leiopathes glaberrima c h 120–800 x x Cnidome described by Bo et al. (2015) Opresko and Baron-Szabo
(Esper, 1788) (2001) and Bo et al. (2015)
Family Myriopathidae
Antipathella subpinnata c h 60–600 x Cnidome described by Bo et al. (2008), Opresko (2001) and Bo et al.
(Ellis & Solander, 1786) who summarised Mediterranean records (2008)
Family Schizopathidae
Parantipathes larix (Esper, c h 90–2200 x x Cnidome described by Bo et al. (2014) Opresko and Baron-Szabo
1790) (2001) and Bo et al. (2014)
Order Scleractinia Zibrowius (1980)
Family Caryophylliidae
Anomocora fecunda c h ~200–300 Last deep-sea scleractinian added to the
(Pourtalès, 1871) Mediterranean fauna inventory (Pardo et al.
2011; OCEANA 2014)
Caryophyllia calveri s h 100–800
Duncan, 1873
Caryophyllia cyathus (Ellis s h 65–300 x
& Solander, 1786)
Caryophyllia inornata s h 0–443 x Lower depth limit in the Gibraltar area
(Duncan, 1878) (Álvarez-Pérez et al. 2005). Mostly
occurring shallower than 50 m depth
Caryophyllia smithii Stokes s h, ~5–400+ Mostly occurring shallower than 50 m
& Broderip, 1828 sb depth. Lower depth limit corresponds to the
Alboran Sea
Ceratotrochus magnaghii s h 7–400 x x Shallow depth limit corresponds to
Cecchini, 1914 submarine caves (Zibrowius 1980)
Coenocyathus c h 35–200 x
anthophyllites Milne
Edwards & Haime, 1848
Coenocyathus cylindricus c h 65–600 ? Probably first described from the
Mine Edwards & Haime, Mediterranean Sea (Zibrowius 1980)
1848
Desmophyllum dianthus s h 30–1257 x Shallow depth limit in the Gibraltar area
(Esper, 1794) (Álvarez-Pérez et al. 2005)
Hoplangia durotrix Gosse, c h 0–150 Mostly occurring shallower than 50 m
1860 depth
Lophelia pertusa (L., 1758) c h 39–1100 x Shallow depth limit in the Gibraltar area
(Álvarez-Pérez et al. 2005)
Paracyathus pulchellus s h ~7–220 x Mostly occurring shallower than 50 m
(Philippi, 1842) depth
Pourtalosmilia c h 100+ (?) ? Probably first described from the
anthophyllites (Ellis & Mediterranean Sea (Zibrowius 1980).
Solander, 1786) Scarce reliable depth data on live colonies
available
Thalamophyllia gasti c h 13–610+ x Shallow depth limit corresponds to
(Döderlein, 1913) submarine caves (Zibrowius 1980)
Family Dendrophylliidae
Balanophyllia cellulosa s sb 80–320
Duncan, 1873
(continued)
Dendrophyllia cornigera c h 72–733 x
(Lamarck, 1816)
Dendrophyllia ramea (L., c h 30~240 x Lower depth limit corresponds to the
1758) Menorca channel (Jiménez et al. 2016)
Leptopsammia pruvoti s h ~5–150 x Mostly occurring shallower than 50 m
Lacaze-Duthiers, 1897 depth
Family Flabellidae
Javania cailleti s h 400–660
(Duchassaing & Michelotti,
1864)
Monomyces pygmaea s h 5–150 x Mostly occurring shallower than 50 m
(Risso, 1826) depth
Family Guyniidae
Guynia annulata Duncan, s h, ~5–300+ x Shallow depth limit corresponds to
1872 sb submarine caves
Family Stenocyathidae
Stenocyathus vermiformis s h, 43–1350 Shallow depth limit in the Gibraltar area
(Pourtalès, 1868) sb (Álvarez-Pérez et al. 2005)
Family Oculinidae
Madrepora oculata L., c h 33–1100 x x Shallow depth limit in the Gibraltar area
1758 (Álvarez-Pérez et al. 2005)
Family Turbinoliidae
Sphenotrochus andrewianus s sb 10–187 Lower depth limit corresponds to the
Milne Edwards & Haime, Gibraltar area (Álvarez-Pérez et al. 2005).
1848 Mostly occurring shallower than 50 m
depth
Scleractinia Incertae Sedis
Cladocora debilis Milne c sb 24–480
Edwards & Haime, 1849
Order Zoantharia
Family Parazoanthidae
Savalia savaglia (Bertoloni, c h 15–900 x Last new deep-sea coral zoanthid described Lacaze-Duthiers (1864a) and
1819) from the Mediterranean Sea Ocaña and Brito (2004)
Subclass Octocorallia
Order Alcyonacea
Suborder Alcyoniina
Family Alcyoniidae Weinberg (1977)
Alcyonium acaule Marion, c h 10–125 * x Mostly occurring shallower than 50 m Verseveldt (1964)
1878 depth
Alcyonium coralloides c h 0–135 x Mostly occurring shallower than 50 m
(Pallas, 1766) depth
Alcyonium palmatum c sb 20–700 x Verseveldt (1964)
Pallas, 1766
Anthomastus sp. c h 400–500 As Anthomastus cf. grandiflorus No description of this species
(OCEANA 2014). Last deep-sea available. See Fig. 14.6A–B
alcyonacean added to the Mediterranean
fauna inventory. Only in the Alboran Sea
Family Nidaliidae
Chironephthya c h 115–200 x x Last new deep-sea alcyonacean described López-González et al. (2014)
mediterranea López- from the Mediterranean Sea
González, Grinyó & Gili,
2014
Nidalia studeri (von Koch, c h 100–329 x x López-González et al. (2012)
1891)
Family Paralcyoniidae
Paralcyonium spinulosum c h 15–300+ x Mostly occurring shallower than 50 m Weinberg (1977)
(Delle Chiaje, 1822) depth
Suborder Calcaxonia
Family Dendrobrachiidae
(continued)
Dendrobrachia bonsai c h 200–1080 D. fallax Brook, 1889 records correspond López-González and Cunha
López-González & Cunha, to this species (2010) and Sartoretto (2012)
2010
Family Ellisellidae Grasshoff (1972) and
Weinberg and Grasshoff
(2003)
Ellisella paraplexauroides c h 15–200 Angiolillo et al. (2012)
Stiasny, 1936
Nicella granifera c h ~100–400+ Only in the Alboran Sea?
(Kölliker,1865)
Viminella flagellum c h 70–400+ x
(Johnson, 1863)
Family Isididae
Acanella arbuscula c sb 300–800 ? Probably habitat-forming. Further studies Saucier et al. (2017)
(Johnson, 1862) needed
Acanella furcata Thomson, c sb 190–1000 ? x x Probably habitat-forming. Further studies Thomson (1929) and Saucier
1929 needed et al. (2017)
Isidella elongata (Esper, c sb 115–1656 x * x Weinberg and Grasshoff
1788) (2003)
Family Primnoidae
Callogorgia verticillata c h 90–1000 x x Carpine and Grasshoff (1975)
(Pallas, 1766) and Weinberg and Grasshoff
(2003)
Suborder Holaxonia
Family Acanthogorgiidae Grasshoff (1973)
Acanthogorgia armata c h 150–500+ Only in the Alboran Sea
Verrill, 1878
Acanthogorgia hirsuta c h 100–924 Carpine and Grasshoff (1975)
Gray, 1857
Family Gorgoniidae Carpine and Grasshoff (1975),
Weinberg (1976), Grasshoff
(1988, 1992) and Weinberg
and Grasshoff (2003)
Eunicella cavolini (von c h 10–186+ x x Mostly occurring shallower than 50 m
Koch, 1887) depth
Eunicella filiformis (Studer, c sb 45–250 Only in the Alboran Sea
1878)
Eunicella singularis (Esper, c h 10–100+ * x Two morphotypes have been described, one
1791) proper of deeper depths lacking
zooxanthellae (Costantini et al. 2016).
Mostly occurring shallower than 50 m
depth
Eunicella verrucosa (Pallas, c h ~5–200 x Mostly occurring shallower than 50 m
1766) depth
Filigorgia guineensis c sb 250–300 Only in the Alboran Sea Ocaña et al. (2000a)
(Grasshoff, 1988)
Leptogorgia sarmentosa c h ~5–300 ? Probably first described from the
(Esper, 1789) Mediterranean Sea. Mostly occurring
shallower than 50 m depth
Family Plexauridae Carpine and Grasshoff (1975),
Grasshoff (1977) and
Weinberg and Grasshoff
(2003)
Bebryce mollis Philippi, c h 100–250+ x
1842
Muriceides lepida Carpine c h 80–718 x
& Grasshoff, 1975
Paramuricea clavata c h 35–110+ * x Mostly occurring at 50–60 m depth
(Risso, 1826) (Carpine and Grasshoff 1975)
(continued)
Paramuricea macrospina c h 40–300+ x x
(Koch, 1882)
Placogorgia coronata c h ~200–1000 x Differentiation of Paramuricea and
Carpine & Grasshoff, 1975 Placogorgia needs molecular evaluation
Placogorgia massiliensis c h 350–500 x
Carpine & Grasshoff, 1975
Spinimuricea atlantica c h 50–96 Only in the Alboran Sea
(Johnson, 1862)
Spinimuricea klavereni c h 50–80 x x
(Carpine & Grasshoff,
1975)
Swiftia pallida Madsen, c h 100–600 Swiftia needs revision. Possible cryptic
1970 species
Villogorgia bebrycoides c h 100–300+ x
(von Koch, 1887)
Suborden Scleraxonia
Family Coralliidae
Corallium rubrum (L., c h 3–800 x Carpine and Grasshoff (1975)
1758) and Weinberg (1976)
Suborder Stolonifera
Family Clavulariidae
Clavularia carpediem c h 40–200 x x Doubtful generic adscription. Mostly Weinberg (1986) and
Weinberg, 1986 occurring shallower than 50 m depth López-González (1993)
Clavularia marioni von c h 70+ x An extremely rare species. Doubtful Weinberg (1978)
Koch, 1891 generic adscription
Rolandia coralloides c h 0–800 (?) x Mostly occurring shallower than 50 m Ocaña et al. (2000b)
Lacaze-Duthiers, 1900 depth
Sarcodictyon catenatum c h 0–100 Mostly occurring shallower than 50 m Ocaña et al. (2000b)
Forbes, 1847 depth
Scleranthelia rugosa c h 200–714 Carpine (1964, as
(Pourtalès, 1867) Scleranthelia musiva Studer,
1878)
Telestula septentrionalis c h 600–700 Description of the Mediterranean Madsen (1944)
Madsen, 1944 specimens needed
Order Pennatulacea Kükenthal (1915), Gili and
Pagès (1987) and Williams
(1995) (diagnoses of genera)
Family Funiculinidae
Funiculina quadrangularis c sb 70–616 x x
(Pallas, 1766)
Family Kophobelemnidae
Kophobelemnon stelliferum c sb 70–618 x K. leuckartii Cecchini, 1917 is a synonym Mastrototaro et al. (2013)
(Müller, 1766) (Mastrototaro et al. 2013)
Family Pennatulidae
Pennatula aculeata c sb 150–300
Danielssen, 1860
Pennatula phosphorea L., c sb 30–570
1758
Pennatula rubra (Ellis, c sb 20–200+ x Abdelsalam (2014)
1761)
Pteroeides spinosum (Ellis, c sb 20–280 x Abdelsalam (2014)
1764)
Family Protoptilidae
Protoptilum carpenteri c sb 240–451 Last sea-pen added to the Mediterranean Mastrototaro et al. (2014)
Kölliker, 1872 fauna inventory
Family Veretillidae
Cavernularia pusilla c sb 14–200 x Last new sea-pen described from the Abdelsalam (2014)
(Philippi, 1835) Mediterranean Sea
(continued)
Veretillum cynomorium c sb 15–260 x Shallow depth limit from Alboran Sea
(Pallas, 1766) (Ocaña et al. 2000a)
Family Virgulariidae
Virgularia mirabilis c sb 7–620 Shallow depth limit from Alboran Sea
(Müller, 1776) (Ocaña et al. 2000a)
Class Hydrozoa
Subclass Hydroidolina
Order Anthoathecata
Suborder Filifera
Family Stylasteridae
Errina aspera (L., 1767) c h 61–443 x x Last new stylasterid described from the Zibrowius and Cairns (1992)
Mediterranean Sea
(A) Coloniality: s solitary species, c colonial species
(B) Substrate: h hard-bottom species, sb, soft-bottom species
(C) Depth range (m)
(D) Habitat-forming species in the Mediterranean Sea at depths >200 m (see Chimienti et al., this volume)
(E) Mediterranean endemics (* Near-endemic, occurs also in nearby Atlantic waters)
(F) Species that was first described in the Mediterranean Sea. Species reference: papers in which Mediterranean material of the species concerned
is described. Bibliographic references in cells corresponding to taxa higher than genus (family, order, etc.) means that most, if not all, species/
genera in these taxa are described in the corresponding paper. For instance, all scleractinian corals (order Scleractinia) are described in Zibrowius
(1980). In the Scleractinia, depth range refers to live specimens whenever this information was available
Fig. 14.4 (a) Antipathella

subpinnata, Chella Bank,
Alborán Sea off Spain, 330 m.
(b) Antipathes dichotoma,
Balearic Islands, 550 m. (c)
Leiopathes glaberrima,
Chella Bank, 400 m. (d)
Parantipathes larix, Cabliers
Bank, Alborán Sea, 420 m.
(Photographs: © OCEANA)
the lower part of the corallum arranged in alternating groups cally and nearly parallel to each other, with branchlets along
along the sides of the stem (Opresko 2002). The type was the stem and lower order branches mostly directed distally
thoroughly re-described by Opresko and Baron-Szabo (Fig. 14.4a). Antipathes dichotoma was re-described by
(2001). According to these authors, further studies are Opresko (2003) based on a specimen from Naples. According
needed in order to determine whether Mediterranean speci- to this author, the corallum may reach 1 m in height or more,
mens with shorter pinnules are indeed P. larix or whether and the ramification is sparse. The branches are long and
they represent a separate species. The morphological descrip- flexible disposed irregularly on all sides of the stem and
tions of A. subpinnata in the literature are frequent (see a lower order branches (Fig. 14.4b). Finally, A. fragilis is an
review by Bo et al. 2008). A neotype was thoroughly obscure poor known species whose type was lost. The type
described by Opresko (2001). The corallum reaches over 1 m was a fragment, so even the colony size is unknown. Colonies
in height, and is of a whitish colour underwater (see Bo et al. attributed to this species were recently observed at 600 m
2008). It consists of several elongate branches arising verti- depth (Fabri and Pedel 2012).
Remarkable Sites and Distribution area with the highest diversity known so far in the Spanish
The Mediterranean antipatharians occur on shoals and rocky Mediterranean Sea. We refer to other chapters in this book
cliffs (where they can constitute monospecific populations), for descriptions and locations of the newly discovered
on the shelf and at bathyal depths associated to white corals communities.
(developing mixed populations with other anthozoans), or
sparse in the canyons (Bo et al. 2015). Bo et al. (2008, 2011, 14.3.1.2 Order Scleractinia
2012a, 2014, 2015) and Ingrassia et al. (2015) described Scleractinians are marine solitary or colonial cnidarians that
populations following these criteria. account for 1482 extant species among which 615 are con-
Antipathella subpinnata, A. dichotoma and L. glaberrima sidered deep-sea corals (Cairns 2007). These corals are eco-
are widely distributed in the Mediterranean Sea, and accord- logical important components as they shape the diversity of
ing to Bo et al. (2008) the former is probably the most com- both shallow water environments and the deep-sea habitats.
monly observed in this area. Parantipathes larix is considered Scleractinian polyps are similar to the model already
uncommon (Bo et al. 2014). A distribution map of A. dicho- described in the Subclass Hexacorallia. They have mesenter-
toma with compilation of all records was given by Bo et al. ies arising in pairs and arranged in cycles. The external skel-
(2011). In Vafidis (2010) and Chimienti et al. (this volume) eton made of aragonite (corallum) has vertical partitions
comprehensive information on distribution as well as maps (septa) arising from the basal plate that form cycles and
are included. Following these authors, all five species are occur between the mesenteries (Fig. 14.1). Stony corals,
known from the western basin, four are known from the including the Mediterranean species, have been deeply
Aegean Sea (A. fragilis not recorded), two from the Adriatic investigated through time. Studies on the anatomy of the
Sea (A. subpinnata, L. glaberrima) and two from the Ionian skeleton and on the morphological features were performed
basin (A. dichotoma, L. glaberrima). All species (excepting by Vaughan and Wells (1943) and Wells (1956).
A. fragilis) inhabit both shelf and slopes in the Mediterranean Recent papers on the microstructure and genetic diversity
basin (Table 14.2). An exceptional record of P. larix at of these organisms contributed to shed light onto their sys-
2200 m was recently given by Fabri and Pedel (2012). tematics, and the taxonomy of numerous taxa was revised
The bay of Naples is the type locality for three of the five (Stolarski 2000; Stolarski and Roniewicz 2001; Budd et al.
Mediterranean deep-sea species that were first described 2010). Molecular phylogenies and morphological studies are
from Naples in the eighteenth century (A. fragilis, L. glaber- not necessarily congruent. The monophyly of the five “tradi-
rima, P. larix). Opresko (2001, 2003) chose specimens col- tional” suborders (i.e. Astrocoeniina, Caryophylliina,
lected in the bay for the description of neotypes of A. Faviina, Fungiina and Dendrophylliina) based on morphol-
dichotoma, and A. subpinnata, whose types were lost. The ogy (Wells 1956) is not always supported by molecular stud-
bay is also the type locality of two species described by von ies (Budd et al. 2010). Therefore, different morphological
Koch (1889) now considered not valid (Antipathes aenea characters are being tested to better explore the systematics
and Antipathes gracilis). In addition, L. glaberrima is also of these groups (Budd and Stolarski 2009).
the type species of the genus Leiopathes, A. dichotoma of the We refer to Stolarski and Roniewicz (2001) for a review
Order Antipatharia, P. larix of the genus Parantipathes, and of the evolutionary relationships and classification of the
A. subpinnata of the genus Antipathella (see Opresko 2001; Scleractinia.
Opresko and Baron-Szabo 2001). The fauna of Naples was
described thoroughly in several papers (von Koch 1889; Taxonomy and Taxonomic Characters
Gravier 1918; Opresko and Baron-Szabo 2001; Opresko Taxa discrimination is substantially based on different fea-
2003) and material from this area was used in the key-work tures of the skeleton (corallum) at three levels: macromor-
of Brook (1889). phology, micromorphology and microstructure (see Budd
Due to the extended use of remotely operated vehicles and Stolarski 2009; Budd et al. 2010). However, some fea-
(ROVs), exceptional antipatharian facies are being discov- tures exhibit intraspecific variation, and the study of large
ered mainly in the Italian waters of the western basin (Bo series of specimens leads reductions in terms of valid species
et al. 2014, 2015; Angeletti et al. 2014; Ingrassia et al. 2015), and complicated synonymies (Zibrowius 1984). Despite
demonstrating that black corals are much more abundant exhibiting convergence, most traditional macro-
than previously thought (see Bo et al. 2008, 2012b, 2015). morphological characters have been used to define genera
Four of the Mediterranean species have been identified in and families (Kitahara et al. 2016) making their taxonomy
Chella Bank (Alborán Sea off Spain), a site with a rich fauna. even more complicated. Morphological variability includes:
Antipatharians were recorded as deep as the 500–600 m growth form in colonial species or shape of the corallum in
interval (Fig.14.4a, c; OCEANA 2014). This is probably the solitary ones, coenosteal development, and size of the caly-
ces. Calicinal structures also vary, as well as the number of and morphological similar caryophylliids, showed phyloge-
septa and their width or exsertness, development of the colu- netic affinity between some Dasmosmilia, Crispatotrochus
mella, pali, symmetry of the radial structures, or the arrange- and Caryophyllia species (Kitahara et al. 2010a). Indeed the
ment of septa according to Pourtalès plan in the Mediterranean species C. inornata was placed in a group
dendrophylliids (septa fused forming triangles, see comprising three congeneric species and Crispatotrochus
Fig. 14.1b, Table 14.3 and Cairns 2001). Zibrowius (1984) rugosus. The other Mediterranean species included in the
proposed the use of new characters for the azooxanthellate dataset, P. pulchellus, was sister to Polycyathus muellerae, a
scleractinians taxonomy and reconsidered other characters shallow-water coral occurring also in the Mediterranean Sea.
such as the attachment structures, the spatial relationships of Although the majority of shallow-water scleractinian fami-
calicular elements, septal ornamentation and the type of lies are polyphyletic, Arrigoni et al. (2014) confirmed the
asexual reproduction. Overall soft tissues and cnidome are monophyly of Dendrophylliidae using molecular phylogeny,
not very useful for genus or species level identifications. micromorphology and skeleton microstructure. In their
However, Terrón-Sigler and López-González (2005) anal- study, sequences of five Mediterranean species were
ysed the cnidome of two Mediterranean shallow-water included, two of which Dendrophyllia cornigera and L. pru-
Balanophyllia, showing its usefulness for taxonomic deter- voti occur in deep waters, although the latter is of predomi-
minations among congeneric species. Little is so far known nant shallow-water occurrence. Genetic studies on the
about the deep-sea species. Mediterranean Desmophyllum dianthus and Lophelia per-
Vaughan and Wells (1943) keyed all scleractinian taxa tusa have been performed by Addamo et al. (2012, 2015), but
until genus level, Kitahara et al. (2010a) worked on see also Boavida et al. (this volume). Addamo et al. (2012)
Caryophyllia species and provided identification keys, sequenced two nuclear (ITS and 28S rRNA) and two mito-
whereas Cairns and Kitahara (2012) explained and depicted chondrial (16S rRNA and COI) markers of several deep-sea
all the morphological characters currently used for the scleractinians, among which some were collected in the
description of the azooxanthellate species and keyed all gen- Mediterranean Sea. Although mostly from the North-eastern
era. We refer to Zibrowius (1980) for descriptions, ecology, Atlantic, there are several molecular studies available on
distribution and literature of all Mediterranean species. population genetics of L. pertusa (Le Goff-Vitry et al. 2004a;
Le Goff-Vitry and Rogers 2005; Dahl 2013). Comparative
Molecular Aspects analyses among complete mitochondrial genomes of
Genetic studies on Mediterranean deep-sea scleractinians are Mediterranean and Norwegian L. pertusa populations were
available only for a few species, although recent phyloge- done by Flot et al. (2013). Regarding the mitochondrial
netic studies include some of them. For instance, molecular DNA, few complete mitogenomes of Mediterranean deep-
data of 12 Mediterranean species, seven of them included in sea scleractinians were until now sequenced and published
the present chapter (Caryophyllia inornata, Ceratotrochus (i.e., D. dianthus by Addamo et al. 2016; M. oculata by Lin
magnaghii, Guynia annulata, Leptopsammia pruvoti, et al. 2012, and L. pertusa by Emblem et al. 2011).
Monomyces pygmaea, Paracyatus pulchellus and Significant changes in the phylogenetic relationships are
Thalamophyllia gasti), were considered for evolutionary expected whenever more studies using different molecular
studies (Romano and Cairns 2000). Additionally, Daly et al. markers become available. In the meantime, the current ten-
(2003) and Le Goff-Vitry et al. (2004b) explored the use of dency in scleractinian taxonomy is to avoid a subordinal
mitochondrial 16S ribosomal RNA from some of these spe- classification.
cies for phylogenetic reconstructions within Hexacorallia
and Scleractinia, respectively. The genetic structure of sev- Mediterranean Species
eral Mediterranean populations of L. pruvoti was investi- Thirty deep-water scleractinians belonging to seven families,
gated by Goffredo et al. (2009), yet the molecular data and an additional species of uncertain taxonomic ascription
available for other Mediterranean scleractinians concerns (Cladocora debilis, see Hoeksema and Cairns 2013), are
shallow-water species only. One of the most comprehensive known from the Mediterranean basin. Among these, five
phylogenetic analyses of the order was based on COI (see have only been collected dead, with a definitely fossil aspect
Kitahara et al. 2010b). In Kitahara’s et al. study, more than or included in lithified sediment (Caryophyllia ambrosia, C.
200 taxa representing both shallow and deep-sea species, atlantica, C. sarsiae, Schizocyathus fissilis, Trochocyathus
from 25 scleractinian families, were analysed. However, mediterraneus) (Zibrowius 1980; Pardo et al. 2011; Taviani
among the taxa investigated, only two species occur in the et al. 2011; Vertino and Corselli, this volume) and therefore
Mediterranean Sea (Madrepora oculata, Stenocyathus ver- cannot be considered part of the extant fauna or definitely
miformis). The phylogenetic tree revealed that most of the extinct. Only one species is endemic (C. magnaghii), and
families are polyphyletic. Subsequent analyses, based on four are considered CWCs: D. cornigera, D. dianthus, L.
partial mitochondrial 16S rRNA, performed on Caryophyllia pertusa and M. oculata (see Chimienti et al., this volume and
Table 14.3 Some morphological characteristics of the Mediterranean deep-sea Scleractinia
Pali/
Corallum Maximal paliform
Species Corallum shape Colony form attachment GCD (mm) Columella lobes Septal cycles Remarks
Family
Caryophylliidae
Anomocora fecunda Colonial Elongate and a 12 Trabecular P2–P3 S1–S4 Budded corallites detach from parent
cylindrical
Caryophyllia Cylindrical/ – a 12 Variable, Absent/P3 S1–S5 Can form small pseudocolonies by
inornata turbinate fascicular fixation of juveniles on adults. S5 rarely
complete
Caryophyllia calveri Cylindrical/ – a/f 15 Fascicular P3 S1–S4 Septa arranged decamerally or
turbinate hexamerally
Caryophyllia Cylindrical/ – a 30 Fascicular P4 S1–S5
cyathus turbinate
Caryophyllia smithii Cylindrical/ – a/f 35 Fascicular/spongy P3 S1–S5 S5 rarely complete
trochoid
Ceratotrochus Cylindrical – a 8 Trabecular Absent S1–S4
magnaghii
Coenocyathus Colonial Phaceloid a 11 Papillose P3 S1–S4 Exceptionally, a few S5
cylindricus
Coenocyathus Colonial Phaceloid a 9 Papillose Absent S1–S4
anthophyllites
Desmophyllum Cylindrical/flared – a 80 Absent/a few rods Absent S1–S5 Corallum highly variable; GCD in
dianthus Mediterranean specimens smaller
14 Taxonomy, Genetics and Biodiversity of Mediterranean Deep-Sea Corals
Hoplangia durotrix Colonial Incrusting/ a 6 Absent Absent S1–S4 Exceptionally, a few S5

slightly ramified
Lophelia pertusa Colonial Dendroid a 15 Absent/a few rods Absent Septa not arranged
in regular systems
Paracyathus Cylindrical/ – a 20 Papillose P1–P4 S1–S5 S5 rarely complete
pulchellus trochoid
Pourtalosmilia Colonial Bushy a 11 Fascicular (P2) P3 S1–S4 Exceptionally, a few S5
anthophyllites
Thalamophyllia gasti Colonial Reptoid a 6 Absent Absent S1–S3
Family
Dendrophylliidae
Balanophyllia Trochoid – a/f 22 Spongy/fascicular Absent S1–S4
cellulosa
Dendrophyllia Colonial Bushy a 22 Spongy Absent S1–S4
cornigera
Dendrophyllia Colonial Arborescent a 16 Spongy/papillose Absent S1–S4
ramea
(continued)
133
134
Pali/
Corallum Maximal paliform
Species Corallum shape Colony form attachment GCD (mm) Columella lobes Septal cycles Remarks
Leptopsammia Turbinate/ – a 17 Spongy Absent S1–S5 Septa not arranged according to
pruvoti cylindrical Pourtalès plan in adult stage. S5 rarely
complete
Family Flabellidae
Javania cailleti Ceratoid – a 40 Fusion of axial Absent S1–S4 Subfossil specimens up to 65 mm in
edges of S1–S2 GCD
Monomyces Cylindrical/ – a 24 Papillose Absent S1–S4 (S5) Attachment reinforced by rootlets
pygmaea conical/
compressed
Family Guyniidae
Guynia annulata Cylindrical, – a/f 1.4 A single ribbon Absent S1–S2 Septa octamerally arranged
scolecoid
Family
Stenocyathidae
Stenocyathus Cylindrical, – a/f 4 Absent/1–3 P2 S1–S3
vermiformis vermiform twisted ribbons
Family Oculinidae
Madrepora oculata Colonial Dendroid a 4 Absent/spongy Absent S1–S3
Family Turbinoliidae
Sphenotrochus Cuneiform – f ~6 Lamellar Absent S1–S3
andrewianus
Scleractinia Incertae
Sedis
Cladocora debilis Colonial f 3 Papillose (P1) P2 S1–S3 The colony lives attached in young
stages
Px, Sx Pali and septa of cycle designated by numerical script, a corallum attached, f corallum free
For an explanation of the terminology we refer to Cairns and Kitahara (2012), and for full descriptions and iconography of the species we refer to Zibrowius (1980)
A. Altuna and A. Poliseno
Table 14.2). No less than 11 of the extant species were first bushy colony with sparse irregular branching (Zibrowius
described from the Mediterranean Sea, most of them during 1980). According to Zibrowius (1980, 2003), these two spe-
the eighteenth and nineteenth centuries (Table 14.2). cies differ in geographical and depth distribution; D. ramea
Our knowledge of the scleractinian deep-water corals is abundant in the southern area of the western basin at
diversity could be considered satisfactory since the mono- 40–75 m depth, whereas D. cornigera has a larger occur-
graph of Zibrowius (1980). Thus, and despite new research rence (including the Aegean Sea) with a bathymetric distri-
undertaken in poorly studied deep-sea areas (e.g., Galil and bution ranging from 80 to 600 m (see a distribution map in
Zibrowius 1992; Mastrototaro et al. 2010; Angeletti et al. the chapter by Chimienti et al., in this volume). However,
2014; Bo et al. 2011, 2012a, 2015), very little has been added recent discoveries revealed the presence of D. ramea in
in terms of biodiversity to Zibrowius’ results, with only deeper locations (between 125 and 170 m) off Cyprus in the
Anomocora fecunda newly recorded from the Alborán Sea Levantine Mediterranean (Orejas et al. 2017) and in the
(Pardo et al. 2011; OCEANA 2014). The latest new species Menorca channel (~240 m, Jiménez et al. 2016). The coral-
discovered from the basin was also described in this paper lum of Balanophyllia and Leptopsammia is solitary. They
(Zibrowius 1980, T. mediterraneus, only dead specimens differ from each other principally for their septa arrange-
known). ments according to Pourtalès plan in the adult (Balanophyllia),
Caryophylliidae is the most diverse Mediterranean fam- or in a normal insertion pattern (Leptopsammia).
ily, with 14 extant species distributed in 10 genera. Similar to Balanophyllia cellulosa is an uncommon coral with a fragile
other families, monophyly is not supported (Daly et al. 2007) skeleton that lives on soft-bottoms, while L. pruvoti is very
and future taxonomic changes may apply whenever addi- abundant. It lives from rather shallow depths down to subma-
tional integrated morphological and molecular studies are rine canyons at 100–150 m (Zibrowius 1980).
undertaken. Anomocora, Coenocyathus, Hoplangia, Species of the family Flabellidae are epithecate solitary
Lophelia, Pourtalosmilia and Thalamophyllia include colo- corals lacking costae but usually bearing chevron-shaped
nial corals. Caryophyllia, Ceratotrochus, Desmophyllum and growth ridges that peak at major septa (Cairns 2000). This
Paracyathus are solitary. Apart from Caryophyllia smithii family includes two Mediterranean species occurring in
that may thrive on both hard- and soft-bottoms (“Caryophyllia deep-water, Javania cailleti and M. pygmaea, with the latter
clavus”, see Zibrowius 1980), all extant Caryophyllia are, living mostly at shallow depths. Both are distinguished by
after the current knowledge, hard-bottom corals. their habitat and external morphology (Table 14.3). Javania
Mediterranean caryophylliids can be distinguished by the cailleti is an uncommon bathyal coral living at 400–660 m
external features of the skeleton (Fig. 14.1a, Table 14.3). As depth that can grow up to 70 mm in height (Zibrowius 1980).
for the colonial species, calicular structures of Coenocyathus The corallum has a long pedicel, a flared calyx with highly
are similar to Caryophyllia, differing only from the fact that exsert septa, and a snow-white and porcelaneous wall.
they form small phaceloid colonies. Both Coenocyathus spe- Monomyces pygmaea is smaller in size, up to 27 mm in
cies (C. cylindricus, C. anthophyllites) are uncommon and height, and has a wall with horizontal ridges. The corallum is
poorly known. Lophelia pertusa has analogous calicular almost cylindrical, of brownish to pinkish colour, and its
structures than D. dianthus, but forms large dendroid colo- attachment is reinforced by rootlets. This coral has been
nies (Fig. 14.5d, f; see Addamo et al. 2016). The morpho- found in the western basin and the Adriatic Sea down to
logical affinity shown by these two genera was also detected 150 m depth (Zibrowius 1980).
under molecular analysis, therefore a taxonomic re-allocation Corals in the families Guyniidae and Stenocyathidae are
of L. pertusa was recently proposed as Desmophyllum pertu- of singular, somehow vermiform morphology, small calicu-
sum (Addamo et al. 2016; Boavida et al., this volume; lar diameter and distinctive skeletal structure. Two species,
Addamo, this volume). G. annulata and S. vermiformis, are widely distributed in the
Species of the family Dendrophylliidae have a porous Mediterranean Sea (Zibrowius 1980). Despite formerly
wall and usually an arrangement of septa in Pourtalès plan included within the family Guyniidae, the singular skeletal
(fusion o septa forming triangles) at least during some stages features of S. vermiformis justified its recent inclusion in a
of the skeletal ontogeny (Cairns 2001) (Fig. 14.1b). Four different family (Stenocyathidae) (see Stolarski 2000).
Mediterranean species live in deep water, namely Guynia annulata inhabits in a broad bathymetric range from
Balanophyllia cellulosa, D. cornigera, Dendrophyllia ramea shallow waters to bathyal bottoms; S. vermiformis is more
and L. pruvoti. Both Dendrophyllia species, commonly restricted to deep-circalittoral and bathyal communities,
known as yellow and pink corals respectively, are colonial, commonly associated to the white coral frameworks,
forming three-dimensional structures growing by extra- although it may be free-living as well (Zibrowius 1980).
tentacular budding on hard bottoms (Figs. 14.1b and 14.5a– Dead, although fresh-looking specimens of S. fissilis
c). Dendrophyllia ramea forms arborescent colonies up to (Schizocyathidae), have been collected by Taviani et al.
1 m in height, while D. cornigera typically has a small and (2011) at ~1120 m depth in the Aegen Sea. Unless live speci-
Fig. 14.5 (a) Dendrophyllia

cornigera (“yellow coral”)
Catifas Bank, Alborán Sea,
400 m. (b) D. cornigera, off
Calahonda, Málaga, 230 m.
(c) Dendrophyllia ramea,
Chella Bank, Alborán Sea,
100 m. (d) Lophelia pertusa,
Cabliers Bank, Alborán Sea,
300 m. (e) Madrepora
oculata, off Malta, 500 m. (f)
Callogorgia verticillata (a)
and L. pertusa (b), off Malta,
850 m. (g) Lophelia pertusa
(a), M. oculata (b), Catifas
Bank, 400 m. (h) White coral
bank with M. oculata and
numerous plexaurids, off
Malta, 700 m. (Photographs:
a–d, g: © OCEANA; e, f, h:
OCEANA/© LIFE BaĦar for
N2K)
mens are discovered, this species can not currently be bottoms (B. cellulosa, C. debilis, S. andrewianus), and three
included in the Mediterranean extant fauna inventory. occur in both types of bottoms (C. smithii, G. annulata, S.
Madrepora oculata is the only deep-sea Mediterranean vermiformis) (Table 14.2). Only one colonial species inhab-
Oculinidae. It forms big-sized colonies whose branches may its soft-bottoms (C. debilis). The scarce number of free-
anastomose acting as substrate and providing refuge to many living Mediterranean scleractinians is worth mention
vagile and sessile organisms (Fig. 14.5e, h). This coral occurs (Table 14.3), particularly if compared with nearby Atlantic
throughout the Mediterranean basin, although is more com- areas (see final Overview).
monly collected dead as often happens with L. pertusa
(Zibrowius 1980). Remarkable Sites and Distribution
The unique Mediterranean turbinoliid is Sphenotrochus Vafidis (2010) reported the geographic distribution of scler-
andrewianus, a small solitary and unattached coral with a actinians along five Mediterranean sectors. In this book there
cuneiform corallum that is adapted to live in the interstices of is also a chapter on the Mediterranean biogeographical dis-
coarse sands (see Cairns 1997). tribution of CWCs (see Chimienti et al., this volume). With
Although was formerly assigned to the families Faviidae 25 known species, the highest diversity is in the western part
and to Caryophylliidae, the current taxonomic placement of of the basin, whereas with only ten species recorded the low-
C. debilis is still uncertain (see Hoeksema and Cairns 2013). est diversity is in the Levantin basin. Given that some of
It builds small colonies formed by extra-tentacular budding. these corals have a broad bathymetrical range (including
Overall, the number of solitary (14) and colonial (11) shallow waters), they probably do not thrive in the deep
Mediterranean deep-sea scleractinians is similar. Differences waters of every sector. Concerning the species that are prin-
are notable in terms of type of substrates, as most species cipally limited to the bathyal zone, the most widely distrib-
inhabit only hard bottoms (19). Only three are typical of soft- uted are L. pertusa and M. oculata, which occur in all five
zones. On the contrary, A. fecunda (newly recorded after zoanthids needs further investigations (see Sinniger and
Vafidis’ review), B. cellulosa and J. cailleti are uncommon Häussermann 2009).
and occur only in one sector.
Lophelia pertusa and M. oculata are of great importance Molecular Aspects
in the deep-sea environments as they are structuring species Molecular analyses using mitochondrial 16S ribosomal RNA
in the so-called “white coral” communities (Pérès and Picard and COI have introduced significant changes in the system-
1964; Zibrowius 2003; Freiwald et al. 2009) (Fig. 14.5h). atics of the order, contributing therefore to the description of
Both species fall into the CWC concept according to their newly proposed genera and species mostly from the Indo-
morphological features and depth distribution. They are Pacific (Sinniger et al. 2010, 2013). In addition, the use of
scarce in the Mediterranean Sea (Taviani et al. 2005) and molecular markers was exploited for the differentiation of
may be considered “relict species” from coldest phases morphologically cryptic species (Kise and Reimer 2016),
(Taviani 2002; Taviani et al. 2011, this volume). Freiwald taxonomic revisions (Risi and Macdonald 2015) and the
et al. (2009) pointed out the 14 known Mediterranean zones assessment of species diversity from different geographic
harbouring live white coral banks. We refer to other chapters areas (e.g., Reimer et al. 2008). The current descriptions of
in this volume for new information and distribution maps of new species in the order are hardly conceived without molec-
these exceptional sites. One of these sites, the Cassidaigne ular comparative analyses.
canyon off Marseille, has been the subject of intensive Molecular analyses on the unique Mediterranean species
research (see Fourt et al., this volume), even by direct obser- (Savalia savaglia) have been done by Sinniger et al. (2007).
vation as early as the late 1950s, and its fauna is one of the Analyses performed on Atlantic individuals of this species
best documented (see Zibrowius 2003). Several species stud- showed no significant differences (Altuna et al. 2010).
ied by Zibrowius (1980) (e.g., M. oculata, C. debilis, C. cal-
veri, C. cyathus), were collected therein. Mediterranean Species
As shown by its colony structure and depth range, S. sava-
14.3.1.3 Order Zoantharia glia (Parazoanthidae) is the only Mediterranean deep-water
This order mostly includes colonial species, many of which coral of the order Zoantharia. A description of the species
interact with other invertebrates establishing different kinds including internal anatomy was given by Lacaze-Duthiers
of associations. Almost all species are soft-bodied, have col- (1864a), Carlgren (1895) and Ocaña and Brito (2004). Ocaña
onies frequently incrusted with sand and other particles, and and Brito (2004) studied the cnidome of individuals from
lack a calcareous or proteinaceous skeleton with the excep- two Mediterranean localities. The species is recognised by
tion of the genus Savalia which has a horny axis. Zoanthid its big-sized yellow, orange or whitish colonies commonly
polyps have two cycles of retractile tentacles, and their inter- ramified in a plane having a horny axis, and soft fleshy pol-
nal anatomy is distinctive, with mesenteries arranged in pairs yps. These are up to 5 mm wide and 6 mm high (preserved
some of which are incomplete (see Häussermann et al. material) and have up to 27 tentacles arranged in two cycles
2003a). (Ocaña and Brito 2004). The systematics of this species has
Zoanthids are distributed worldwide and occur in a wide been problematic, principally due to the axis composition
bathymetric range. Numerous new species will be probably which resembles that of antipatharians. Nevertheless, the
described, as there might be an important cryptic diversifica- anatomy of the polyps, the absence of spines, and the cni-
tion (see Sinniger et al. 2008, 2010, 2013), including the dome indicate that this species belongs to Zoantharia (see
European seas, where a revision of its fauna is needed. Carlgren 1895; Roche and Tixier-Durivault 1951).
Savalia savaglia, called “false black coral”, is a long-
Taxonomy and Taxonomic Characters lived species and probably a slow-growing organism (see
Zoanthids have been traditionally identified based on the Druffel et al. 1995), which colonies create elevated and com-
internal anatomy of the polyps, their external morphology, plex tertiary structures (Cerrano et al. 2010) that may be used
and sometimes also with the aid of the cnidome. For instance, as substrate by other organisms (Lacaze-Duthiers 1864a;
separation between suborders Macrocnemina and Zibrowius 1985a). Cerrano et al. (2010) observed that the
Brachycnemina is based on the presence/absence of perfect presence of S. savalia was associated with a significantly
(macrocnemic) and imperfect (brachycnemic) mesenteries increased availability of substrates and enhanced biodiver-
(see Daly et al. 2007). The body plan is relatively simple and sity. Savalia savaglia commonly shares the habitat with the
many species frequently show remarkable intra-specific sea fan Paramuricea clavata and can cause necrosis covering
plasticity (Alves Santos et al. 2015 and references therein); progressively its axis (Zibrowius 1985b).
thus, species delimitation using external morphological The capability of forming monospecific facies of hun-
characters is often difficult. The utility of cnidome (cnidae dreds of colonies have led to consider S. savaglia as habitat-
types and size ranges) for species discrimination among forming and a vulnerable species. This species is protected in
some of the Mediterranean countries, as was included in the pinnules (pinnule-less species have been described in the
convention for the conservation of European wildlife and Indo-Pacific Ocean, Alderslade and McFadden 2007), eight
natural habitats held in Bern in 1979, and more recently in perfect mesenteries and a single ventral siphonoglyph.
the SPA/BD Protocol of the Barcelona Convention 1995 Polymorphism occurs in some groups.
(Otero et al. 2017; Otero and Marin, this volume). All Mediterranean deep-sea octocorals are colonial and
mostly present calcareous components (sclerites, Fig. 14.2e–
Remarkable Sites and Distribution g) embedded in the tissues, which provide solidity to the
The false black coral has been considered a Mediterranean colony. They are included in two orders, Alcyonacea and
endemic species restricted to the western basin, the Adriatic Pennatulacea whose species have remarkably different mor-
Sea and the Aegean Sea (see Vafidis 2010). However, colo- phologies (Figs. 14.6, 14.7, 14.8, 14.9 and 14.10).
nies were recently identified in some Atlantic sites (Altuna Pennatulaceans are almost exclusively adapted to
et al. 2010). soft-bottoms.
Within the Mediterranean basin, S. savaglia has a bathy- We refer to Hyman (1940), Bayer (1956), Fabricius and
metric range of 15–900 m (Giusti et al. 2015). Its occurrence Alderslade (2001) and Weinberg and Ocaña (2003), for stud-
is better documented from the western basin where is cur- ies on the anatomy and morphological characteristics of the
rently overall uncommon (Zibrowius 1985a, b; Cerrano et al. different orders, families and genera. A glossary including
2010; Giusti et al. 2015). Despite its scarceness, exceptional the morphological and anatomical terms applied to the sub-
populations have been discovered in the Adriatic Sea with class Octocorallia, and a comprehensive illustration with the
hundreds of colonies forming monospecific facies (Giusti different sclerite types were compiled by Bayer et al. (1983).
et al. 2015). Mediterranean records from the Iberian
Peninsula are few and include the Alborán Sea (Pardo et al. 14.3.2.1 Order Alcyonacea
2011). Since it is easily recognisable (due to its morphology The order Alcyonacea constitutes a group of almost exclu-
and size that can exceed one meter in height), the scarcity of sively colonial octocorals including approximately 30 fami-
records in shallow waters seems to reflect its relative rare- lies of soft corals and sea fans (Daly et al. 2007). They are
ness or restriction to deeper depths. This coral may occur morphologically heterogeneous as shown by their colony
elsewhere in the Mediterranean Sea under favorable environ- forms that may include creeping colonies and fleshy masses
mental conditions and protected from human impacts. lacking a skeletal axis, whip-like, fan-like, and tree-like
structures profusely branched and axis of various nature
(Figs. 14.2a–c, 14.6, 14.7 and 14.8). Some species are
14.3.2 Class Anthozoa, Subclass Octocorallia habitat-forming CWCs and can structure single- or multi-
species assemblages (Yesson et al. 2012; Grinyó et al. 2016;
Octocorals are solitary or colonial anthozoans with octomer- Gori et al., this volume).
ous symmetry and varied morphologies, mostly living in Five sub-ordinal divisions of the Alcyonacea include
deep waters (Cairns 2007; Yesson et al. 2012; Pérez et al. Mediterranean species. Although they are not fully supported
2016). Polyps have eight tentacles with lateral extensions or by molecular data (some are polyphyletic groups, see
Fig. 14.6 (a, b) Anthomastus

sp., Cabliers Bank, Alborán
Sea, 350–400 m. (c)
Acanthogorgia sp., off Malta,
745 m. (d) Corallium rubrum,
150 m. (Photographs: a, b, d:
© OCEANA; c: ©
OCEANA/© LIFE BaĦar for
N2K)
Fig. 14.7 (a) Callogorgia

verticillata (a), Eunicella sp.
(b) and Alcyonium sp. (c),
110 m. (b) C. verticillata (a)
and a plexaurid (b), probably
Placogorgia, Balearic Islands,
600 m. (c) Isidella elongata,
Balearic Islands, 460 m. Note
Nephrops (a) on the left. (d)
C. verticillata (a) and
Viminella flagellum (b),
Chella Bank, 330 m. Note
epizoic zoanthid on the
former (c). (e) A V. flagellum
garden, with several other
coral species, Chella Bank,
130 m. (Photographs: ©
OCEANA)
McFadden et al. 2006), they are still adopted for taxonomic lon with a primary polyp producing secondary polyps from
simplicity (Daly et al. 2007). Based on morphology, its wall.
Mediterranean alcyonarians fit into these sub-ordinal groups,
except perhaps for one stoloniferan (Rolandia coralloides), Taxonomy and Taxonomic Characters
which has strong affinity with Alcyoniina (Ocaña et al. Identification of alcyonaceans is frequently difficult due to
2000b). Some authors, however, disagree and do not recog- their plasticity, and the large variability of the taxonomic
nise a “suborder” status for some of these groups. These divi- characters used to distinguish them. The characters useful
sions are: (i) Alcyoniina, whose colonies have polyps arising for other cnidarians such as the internal anatomy and cni-
from a massive, lobate, coenenchymatous mass; (ii) dome are often too uniform and of little help for most octo-
Holaxonia with usually tree-like colonies with a horny axis corals. Bayer (1961) divided the characters used for octocoral
formed by scleroproteinaceous layers around a hollow cen- classification into those pertaining the colony as a whole
tral core (Fig. 14.2a); (iii) Scleraxonia, that have an axial (size and shape, pattern of branching, distribution of polyps,
structure made up of loose to more or less firmly cemented dimorphism), and those related to the skeletal elements (axis
sclerites by a horny material, which may even acquire a structure, sclerites). Taxonomic separation into families is
stony consistency; (iv) Calcaxonia including species that traditionally done by considering the growth form of the
have a solid axis lacking a central hollow core, and non- colony, the structure of the axis (if present), and its composi-
scleritic calcareous (calcite or aragonite) material and (v) tion; identification at genus and species levels is mostly
Stolonifera with simple polyps arising from reticulating based on the shape, size and distribution of the sclerites in
ribbon-like or membranous stolons creeping upon the sub- the different portions of the colony (Daly et al. 2007). In
strate, or forming branching colonies that arise from the sto- some cases, occurrence of certain sclerites is crucial for
Fig. 14.8 (a) Paramuricea

clavata, Balearic Islands,
75 m depth. (b) Paramuricea
macrospina, off Malta, 300 m
depth. Note epibiont brittle
star. (c) Placogorgia sp.,
Chella Bank, Alborán Sea off
Spain, 460 m. (d) Swiftia
pallida, Chella Bank, 255 m.
(e) Close-up image of a CWC
community, with Callogorgia
verticillata (a), Lophelia
pertusa (b), solitary
scleractinians (c,
Desmophyllum?) and
plexaurids (d, Muriceides?),
off Malta, 895 m.
(Photographs: a, c, d: ©
OCEANA; b, e: OCEANA/©
LIFE BaĦar for N2K)
genus-level identification (Bebryce, Ellisella, Eunicella, or near endemics were until now under-investigated. An
Leptogorgia) (Fig. 14.2e–g). exception is represented by Corallium rubrum, whose ecol-
An identification key to the Mediterranean gorgonians ogy, reproduction and genetics were largely explored in the
and descriptions of all the species were given by Carpine andlast decades due to its commercial importance in jewelry
Grasshoff (1975). Additional descriptions were provided by (see Tsounis et al. 2010; Jiménez and Orejas 2017).
Grasshoff (1972, 1973, 1977, 1992), Weinberg (1976), and Population-level studies have been performed aiming to
Weinberg and Grasshoff (2003). Circalittoral Mediterranean investigate the structure and relationships at different bathy-
Alcyoniina and Stolonifera were revised by Weinberg (1977, metric and spatial scales (e.g., Ledoux et al. 2010; Costantini
1978). Except for sea-pens (Pennatulacea), Bayer (1981) et al. 2013; Bramanti et al., this volume and references
published a key for the identification of the octocoral genera
therein). The transcriptome of the red coral has been recently
occurring worldwide. published, broadening therefore our knowledge on popula-
tion and adaptive genetics (Pratlong et al. 2015). The com-
Molecular Aspects plete mitogenome of C. rubrum was sequenced by Uda et al.
The phylogenetic relationships of the Mediterranean alcyo- (2013) along with other precious corals. The Mediterranean
naceans are poorly known, and the studies so far conducted species showed a different gene arrangement compared to
are principally based on shallow water colonies of well- some congenerics and high phylogenetic affinity with a spe-
known species. According to the sequences so far available cies of Paracorallium. These data confirm that a taxonomic
on GenBank, less than 50% of the Mediterranean species revision within Corallidae is required.
have been considered for molecular-based studies. Among Mediterranean specimens of Alcyonium spp. were anal-
these, the majority pertain to shallow-water species. Except ysed for population genetics (McFadden 1999), phylogenetic
for Paramuricea macrospina, most of the deep-sea endemics reconstructions (McFadden et al. 2001), hybdridisation
(McFadden and Hutchinson 2004) and DNA-barcoding sum). Weinberg (1977) revised these species, by depicting
(McFadden et al. 2011). large series of sclerites and by showing differences in the
The genetic structure of Paramuricea clavata, Eunicella colony structures and sclerome. Mediterranean Alcyonium
cavolini and E. singularis was investigated by Valente et al. was also investigated by Verseveldt (1964), who clarified the
(2010), Mokhtar-Jamaï et al. (2011), Costantini et al. (2016) differences between A. acaule and A. palmatum. Alcyonium
and Masmoudi et al. (2016). Costantini et al. (2016) utilised palmatum is a typical sessile species occurring in muddy cir-
Mediterranean colonies of E. cavolini, E. singularis and calittoral communities; it settles on pebbles, shells and other
Eunicella verrucosa for tracing the phylogenetic relation- similar substrates (Pérès and Picard 1964), while A. coral-
ships among Eunicella species. Recently, two mitochondrial loides commonly overgrows on holaxonians such as
markers (mtMutS and COI) were used for phylogenetic com- Eunicella, Leptogorgia and Paramuricea (Carpine and
parisons among a newly described Mediterranean CWC spe- Grasshoff 1975; Weinberg 1975, 1977). Anthomastus sp. is a
cies (Chironephthya mediterranea) and members of the dimorphic mushroom-shaped coral with a short stalk lacking
genera Chironephthya and Siphonogorgia (López-González polyps and a globose capitulum with large autozooids and
et al. 2014). The molecular data showed a strong affinity small siphonozooids (Fig. 14.6a, b). Nidalia studeri, for long
between the Atlantic and Mediterranean forms as already time considered an obscure species, has been recently re-
highlighted for other anthozoans. In this regard, Poliseno described using material collected in the Menorca channel
et al. (2017) recovered Paramuricea polyphletic and the phy- (López-González et al. 2012). This species has a stalk devoid
logenetic tree inferred showed clear divergence between the of polyps and a capitulum with polyps, reminding
two Mediterranean endemic gorgonians P. clavata and P. Anthomastus, but it lacks siphonozooids, and the anthocodial
macrospina. The molecular dating and biogeographic analy- sclerites are arranged in a collaret (‘crown’) and points
ses performed on a set of Atlanto-Mediterranean Paramuricea (Fig. 14.2d) (López-González et al. 2012). In the collaret, the
highlighted the role of geological events such as the sclerites are arranged transversely in a ring below the tenta-
Messinian Salinity Crisis for the speciation and evolution of cles; the points are eight rows of sclerites placed in chevron
the genus in the Mediterranean basin. in the distal part of the anthocodia (see Bayer et al. 1983,
plate 2). The newly described Chironepthya mediterranea
Mediterranean Species was also collected in this channel (López-González et al.
Vafidis et al. (1994) analysed the Mediterranean alcyonacean 2014). Daniela koreni (Nephtheidae) is another obscure spe-
fauna reporting details on the bibliography, the biogeogra- cies in need of evaluation that was collected by von Koch
phy and diversity of these organisms. Subsequently, Vafidis (1891) from the bay of Naples at 100 m depth. A population
(2010) reviewed the previous inventory and listed 41 probably pertaining this species has been observed by López-
Mediterranean alcyonarian species from shallow to deep González et al. (2012) at the same depth off Menorca and
waters. After excluding the shallow water species and adding could be added to the Mediterranean inventory whenever
the new records, the deep-water fauna consists of 40 alcyo- new studies become available.
narians. Three are habitat-building bathyal species at depths Among calcaxonians there are eigth Mediterranean spe-
higher than 200 m (CWCs) (Table 14.2). At least 24 species cies included into four families with different structure of the
were first described from the Mediterranean Sea, and seven axis and morphology of sclerites. The three Mediterranean
were already known in the eighteenth century (Table 14.2). alcyonaceans considered CWCs are calcaxonians
Most are hard-bottom species and only six are adapted to live (Callogorgia verticillata, Isidella elongata, Viminella flagel-
on soft-bottoms (Table 14.2). Calcaxonia, Holaxonia and lum). Family Isididae is exceptional in having a jointed axis
Scleraxonia (the so-called gorgonians or sea fans), are per- in which calcareous internodes are alternated with horny
haps the most “popular” habitat-forming alcyonaceans nodes made of gorgonin. There are three Mediterranean spe-
(Figs. 14.7 and 14.8). Attribution of a given Mediterranean cies in two genera, Acanella arbuscula, A. furcata and I.
species to any of the different suborders, families or genera elongata that inhabit bathyal compact muds and are anchored
is, with some exceptions, not difficult due to their morpho- to the substrate by a root-like base (Fig. 14.7c). Acanella
logical differences. However, species identification is fre- furcata, described by Thomson (1929) and for a long time
quently challenging. considered a synonym of I. elongata (see Carpine and
The Mediterranean Alcyoniina are included in three fami- Grasshoff 1975), has been resurrected by Saucier et al.
lies (Alcyoniidae, Nidaliidae, Paralcyoniidae) differing in (2017). Isidella elongata has been categorised as “critically
colony structure. Paralcyoniidae is the only family character- endangered” in the UICN red list (see Otero et al. 2017;
ised by the capability of its species to retract the polyparium Otero and Marin, this volume). The species in the family
into the base. Among the seven Alcyoniina inventoried, four Primnoidae have scale-like sclerites covering the axis and
were first described in the Mediterranean basin (Alcyonium the polyps. In the wall of the polyps, they are usually arranged
acaule, A. coralloides, A. palmatum, Paralcyonium spinulo- in rows. Callogorgia verticillata has big-sized white pinnate
colonies with polyps arranged in pairs or whorls (Fig. 14.7a, that is rich in small sclerites, principally spindles with whorls
b, d). Ellisellidae comprises three species in three genera of tubercles (Leptogorgia, Filigorgia, see Carpine and
(Ellisella, Nicella and Viminella) having colonies with a Grasshoff 1975, Fig. 14.2f) and balloon clubs (Eunicella,
strongly calcified axis and small sclerites (see Grasshoff Fig. 14.2e). The occurrence of balloon clubs help to quickly
1972; Carpine and Grasshoff 1975; Bayer and Grasshoff identify the species to genus level. Surface mounds, more or
1994) (Fig. 14.7d, e). Apart from the sclerites, differences in less prominent, into which the anthocodia fully retract are
the colony shape of the three genera are marked (see Bayer usually present in the Mediterranean gorgoniids. In
and Grasshoff 1994). Colonies of Viminella are mostly fla- Leptogorgia, retraction of the polyps commonly leaves a slit-
gelliform (Fig. 14.7e) while Ellisella and Nicella have rami- like aperture in the coenenchyme (Fig.14.2b). Species of
fied colonies. Ellisella has several long whip-like branches; Eunicella and Leptogorgia are distinguished from their con-
Nicella repeatedly branch forming usually flabellate colonies geners by the morphology of the colony, colour, and
with short end-branches. The geographic distribution in the sclerome. The colour and pattern of ramification are cer-
Mediterranea Sea of Ellisella paraplexauroides is due to tainly variable in Leptogorgia colonies from the Alborán
Angiolillo et al. (2012). Additionally, the distribution of V. Sea, especially in individuals near the Strait of Gibraltar. If
flagellum was mapped by Giusti et al. (2012). Finally, more than one species occurs, or these variants pertain to the
Dendrobrachiidae comprises a single small-sized species widely distributed L. sarmentosa, should be further explored.
recently described by López-González and Cunha (2010, Eunicella is the Mediterranean alcyonarian genus with the
Dendrobrachia bonsai). The enigmatic genus Dendrobrachia highest diversity. Six species are known and mostly occur at
has a troubling taxonomic history due to its proteinaceous depths shallower than 50 m. Five species may be also found
spiny axis and the lack of sclerites. deeper than this limit (Table 14.2). Within gorgoniids there
Holaxonians are the most diverse among Mediterranen are two free-living species, Eunicella filiformis and F.
deep-water alcyonaceans. They include 18 species in three guineensis (Grasshoff 1988, 1992; Ocaña et al. 2000a), con-
families, Acanthogorgiidae, Gorgoniidae and Plexauridae. sidered a unique feature among Mediterranean
Several species are densely ramified in a plane or form tree- alcyonarians.
like colonies, although no one is considered a Mediterranean Family Plexauridae is polyphyletic (Wirshing et al.
CWC. Usually, little information on the differentiation 2005). It comprises seven genera and ten species of predom-
among the three families is given by the external structure of inant deep-water occurrence (Table 14.2) that commonly
the axis, or the colony shape and branching pattern. have prominent calyces (Fig. 14.2d). The shape of the scler-
Nevertheless, cross sections of the axis show significant dif- ites and their occurrence and arrangement in different parts
ferences in the structure. The Mediterranean holaxonian of the colony (coenenchyme, calyces and anthocodiae) are
families are more easily recognisable by the types of scler- important taxonomic features (Grasshoff 1977). Among the
ites and their arrangement in the polyps (see Carpine and Mediterranean species the sclerites of the anthocodia are
Grasshoff 1975) (Fig. 14.2e–g). neatly arranged into a collaret and points (Fig. 14.2d).
In the Acanthogorgiidae species, polyps are not retractile, Sclerites are frequently big-sized and include characteristic
forming prominent calyces (Fig. 14.6c). Their armature is forms that in some cases allow to promptly identify colonies
very characteristic, with numerous thin and long sclerites to genus level (Carpine and Grasshoff 1975; Grasshoff
arranged in eight rows in chevron in the polyp wall, and long 1977) (Fig. 14.2g). Species identification in some genera is
and thin strongly projecting spines at the base of the tenta- a challenge as morphological characters like colony and
cles (see Grasshoff 1973; Bayer et al. 1983). There are two sclerome are often highly variable. DNA analyses do not
Mediterranean species: Acanthogorgia armata and A. hir- always show significant variations between different mor-
suta that can be distinguished by differences in the coenen- photypes, and in some cases intra- and inter-specific diver-
chymal sclerites. sity may overlap. Genera like Swiftia need a taxonomic
The Gorgoniidae comprises some of the most abundant revision (Fig. 14.8d).
and widely distributed Mediterranean species included in Mediterranean plexaurids occur mainly in deep waters
three genera, Eunicella, Filigorgia and Leptogorgia forming moderately-sized colonies. By contrast, P. clavata
(Fig. 14.2a–c, e, f). These genera can be distinguished by may form robust colonies that can reach heights higher than
their sclerome and colony habitus, with species ramified in a 1 m (Weinberg 1976) (Fig. 14.8a). Branching pattern is vari-
plane (e.g., E. verrucosa), bushy (e.g., Leptogorgia sarmen- able, with some species having densely ramified colonies (P.
tosa), or filiform (e.g., Filigorgia guineensis). Species clavata) and others with only few branches (Spinimuricea
descriptions including SEM images of the sclerome are spp., Swiftia pallida). Paramuricea clavata is a key species
available (see Carpine and Grasshoff 1975; Weinberg 1976; in certain circalittoral communities and it has been recorded
Grasshoff 1988, 1992; López-González 1993). The majority down to 110 m depth (Carpine and Grasshoff 1975). Other
of the Mediterranean gorgoniids have a thick coenenchyme Mediterranean plexaurids (e.g., Bebryce mollis, Muriceides
lepida, Placogorgia coronata, P. massiliensis, Spinimuricea Remarkable Sites and Distribution

atlantica, S. klavereni, Villogorgia bebrycoides) are poorly Several species such as B. mollis, E. cavolini, Clavularia
known as only rarely collected, and their role in the benthic marioni, N. studeri, P. spinulosum, P. macrospina and V.
communities is still understudied. In this respect, recent bebrycoides were first described from the bay of Naples.
studies have shown that some species such as B. mollis may Others were originally described as new species from this
be abundant in the shelf edge and upper slope of the Menorca bay but later disregarded. These include Gorgonia profunda
channel (Grinyó et al. 2016), a site with a high species rich- (= E. verrucosa), Primnoa ellisii (= C. verticillata) or
ness of gorgonians. Paramuricea clavata and P. macrospina Evagora rosea, tentatively ascribed to R. coralloides by
are known to provide substrata to several vagile and sessile Ocaña et al. (2000b).
animals of different phyla (Carpine and Grasshoff 1975). Except for Anthomastus, known only from the Alborán
Scleraxonians in the Mediterranean Sea are limited to a sin- Sea (OCEANA 2014), Alcyoniidae and Paralcyoniidae spe-
gle species. This is the eurybathic, slow-growing, and widely cies are widely distributed in the Mediterranean basin includ-
distributed C. rubrum know as the precious red coral ing the Marmara Sea (Topçu and Öztürk 2015). On the
(Fig. 14.6d). Corallium rubrum is characterised by its usu- contrary, C. mediterranea and N. studeri (Nidaliidae) are
ally red to pink colour in both, axis and cortex and by its uncommon, occurring only deeper than 100 m in the western
sclerome, with the lack of double clubs in the cortex (see basin. The habitat-forming (CWC) C. verticillata and I. elon-
Carpine and Grasshoff 1975; Bayer et al. 1983). The gata are the most widely distributed calcaxonians in the
Corallidae have a continuous massive calcitic axis and loose Mediterranean Sea (see Vafidis 2010). Distribution maps of
sclerites in the polyps and coenenchyme. The axis may both and V. flagellum are given by Chimienti et al., in this
undergo fossilisation as shown by the coral remains and fos- volume. Dendrobrachia bonsai, is certainly uncommon, and
sil records of species and genera (Pleurocorallium) now is known from the Strait of Sicily, Corsica and the Alborán
absent in the Mediterranean Sea. The majority of these fos- Sea (López-González and Cunha 2010; Sartoretto 2012).
sils were identified in Mediterranean deposits of the Upper Among holaxonians, A. hirsuta (Acanthogorgiidae) has been
Miocene and Pleistocene (see Vertino et al. 2010). Corallium largely considered the unique Mediterranean species of the
rubrum is distributed at unusual depths (600–800 m) in the genus occurring only in the western and Ionian basins (Vafidis
Strait of Sicily as shown by Costantini et al. (2010) that 2010), yet A. armata is also known from the Alborán Sea
detected a possible genetic isolation between deep and shal- (Ocaña et al. 2000a; Pardo et al. 2011). Most gorgoniids are
low populations. A monograph on this coral is due to Lacaze- widely distributed in the Mediterranean basin with the excep-
Duthiers (1864b). Carpine and Grasshoff (1975) and tion of the Levantine basin. The depth range of some species
Weinberg (1976) re-described the species and reviewed the (e.g., E. cavolini, E. verrucosa, L. sarmentosa) is also wide,
taxonomic literature. occurring from shallow waters to the bathyal. Eunicella fili-
The six Mediterranean deep-water Stolonifera pertain five formis and F. guineensis occur only in the Alborán Sea (Ocaña
genera of the family Clavulariidae (Clavularia, Rolandia, et al. 2000a). According to Vafidis (2010) all plexaurids are
Sarcodyction, Scleranthelia, Telestula). They are inconspic- present in the western basin, whereas none is known from the
uous species with polyps arising from ribbons or thin mem- Levantine basin. Paramuricea clavata and P. macrospina are
branes that cover the substrate (see Madsen 1944; Weinberg the most widely distributed. Corallium rubrum, is known in
1978, 1986; Ocaña et al. 2000b). Dead remains of another all basins, although in several areas some populations are
one, Scyphopodium ingolfi have been recently collected declining due to over-exploitation (e.g., Bruckner 2009,
(Taviani et al. 2011). However, it is yet to be proven whether Tsounis et al. 2010).The distribution of stoloniferans was
live colonies of this species occur in the Mediterranean Sea. revised by Vafidis (2010). The highest species richness occurs
The circalittoral species were revised by Weinberg (1978), in the western basin, with five out of six deep-water species
who provided detailed descriptions and depicted long series known only therein. Data from other Mediterranean areas are
of sclerites. Ocaña et al. (2000b) have solved long-lasting scarce. The rarest species is T. septentrionalis, whose exclu-
nomenclatural problems in R. and Sarcodyction, suggesting sive bathyal occurrence is reported from a single record in the
the possibility of moving Rolandia coralloides to the Ligurian Sea (Morri et al. 2008).
Alcyoniina. Telestula septentrionalis is characterised by its
branching colonies arising from a band-like stolon and 14.3.2.2 Order Pennatulacea
sclerome (Madsen 1944). The remaining species are differ- Pennatulaceans, commonly known as sea-pens or sea-
entiated principally by the shape and arrangement of the feathers, include 14 worldwide families and ~200 species
sclerites. The North-eastern Atlantic and Mediterranean spe- occurring from shallow to deep waters where they are more
cies attributed to the genus Clavularia differ from the type diversified (Williams 1995, 2011; Daly et al. 2007).
species Clavularia viridis, and their generic position needs Taxonomic revision of several families is still needed and
further evaluation. significant changes may apply.
Fig. 14.9 Pennatula species

from the Mediterranean Sea.
(a, b) P. phosphorea, showing
two colour varieties; MEDITS
2015 Balearic Islands, 99 m
and 138 m depth respectively.
(c) P. rubra, cream specimen;
MEDITS 2015 Balearic
Islands, 99 m depth. (d, e) P.
rubra, red specimens, dorsal
and ventral views showing
peduncle (p), raquis (r) and
polyp leaves (pl); MEDITS
2015, Alborán Sea off
Malaga, 71 m depth. (f) P.
aculeata, Bay of Biscay
specimen, 773 m depth. (g) A
polyp leave from P. rubra
removed from colony; arrow
(a) shows autozooid. (h) Two
autozooids from P.
phosphorea; arrows show
teeth from calyx (t) and
tentacles (te). (i) Autozooid
from P. aculeata; arrows show
tentacles (te) and teeth from
calyx (t). Scale bar: a–
f = 30 mm; g = 5 mm; h,
i = 1 mm
Sea-pens have a very distinctive morphology that reflects We refer to Kükenthal and Broch (1911), Kükenthal
adaptation to the different kinds of sediments. Their colony (1915), and Williams (1995) for thorough accounts of the
structure is the most complex within the Octocorallia, mak- order. Williams (1999) compiled and analysed all the litera-
ing these animals a morphological distinct and discrete taxo- ture on sea-pens, including geographic and subject indexes.
nomic entity. Colonies typically comprise an axial or primary His work includes also the Mediterranean fauna.
polyp (oozooid) differentiated into a muscular, fleshy, basal
peduncle that anchors the animal into the sediments, and a Taxonomy and Taxonomic Characters
distal rachis with numerous secondary polyps that are bud- Families and genera are distinguished on the basis of: (i)
ded from it (Figs. 14.9 and 14.10). Usually the colony has an colony shape; (ii) arrangement of the secondary polyps in
internal, thin, axial rod round or quadrangular in cross- the rachis and their morphology (including presence-
section. Secondary polyps were traditionally divided into absence of calyces in the autozooids and their shapes,
three types according to their morphology (principally dif- Fig. 14.9h, i); (iii) presence or absence of sclerites in the
ferent grades of reduction of the tentacles), which have var- colony or in different parts of it, and (iv) sclerites morphol-
ied functions within the colony. Autozooids capture and ogy (Williams 1995; Daly et al. 2007). Williams (1995) pro-
digest food and provide nourishment and protection to the vided information on the distribution and diversity of
gametes. Siphonozooids produce inhalant currents inflating nominal species, including identification keys for families
the colony. Mesozooids have an exhalant function deflating and genera, and diagnoses of all genera. Diagnoses of fami-
the colony. lies were provided by Kükenthal (1915) and Hickson (1916).
Fig. 14.10 (a) Funiculina

quadrangularis, Chella Bank,
Alborán Sea off Spain, 230 m.
(b) Kophobelemnon
stelliferum, Chella Bank,
600 m. (c) Pennatula rubra,
Balearic Islands, 200 m. (d) P.
rubra, Chella Bank, 125 m.
(e) Pennatula phosphorea;
compare this image of an
inflated colony in situ, with
contracted specimen in
Fig. 14.9a, b. (f) Pteroeides
spinosum, Sicily, 80 m.
(Photographs: © OCEANA)
The world species were keyed by Kükenthal (1915) and Mediterranean Species
those occurring off the Spanish North-western Mediterranean Ten deep-sea pennatulaceans, included in six families, have
Sea by Gili and Pagès (1987). been recorded from the Mediterranean Sea. Two have
habitat-building ability at depths higher than 200 m (CWC),
Molecular Aspects F. quadrangularis and Kophobelemnonm stelliferum (Tables
The systematics and molecular phylogeny of deep-sea pen- 14.2 and 14.4). Five were first described from the
natulaceans were recently investigated by Dolan et al. Mediterranean Sea, four of them in the eighteenth century,
(2013) using six different markers. MtMutS was confirmed and eight were already known by the early twentieth century
the most suitable marker for lower level phylogenetic stud- (Kükenthal and Broch 1911): Cavernularia pusilla, F. quad-
ies as formerly shown by France and Hoover (2001) and rangularis, K. stelliferum, Pennatula rubra, P. phosphorea,
van der Ham et al. (2009). Although four species occurring Pteroeides spinosum, V. mirabilis, Veretillum cynomorium.
in the Mediterranean Sea were analysed (Funiculina quad- Further records include P. aculeata (Thomson 1927) and
rangularis, Pennatula aculeata, P. phosphorea and Protoptilum carpenteri (Mastrototaro et al. 2014, 2017).
Virgularia mirabilis), none of the colonies studied was of Distinction among Mediterranean species is not difficult,
Mediterranean origin. This highlights once again the lack as their colonies show peculiar external features with marked
of molecular data for specimens collected in the differences between the families and most of the genera (see
Mediterranean Sea. The genetic structure of F. quadrangu- Kükenthal and Broch 1911; Kükenthal 1915) (Table 14.4).
laris from Scotland as well as other European areas was Within the ten deep-sea Mediterranean species, half have
studied by Wright et al. (2014). isolated autozooids arising directly from the rachis (C.
The systematics of the order established by Kükenthal pusilla, V. cynomorium, F. quadrangularis, K. stelliferum, P.
and Broch (1911) and Kükenthal (1915), mostly based on carpenteri), whereas the others have autozooids grouped in
external features of the colony, has been proven to be inade- leaves arranged alternately in two opposite rows (P. acu-
quate at sub-ordinal, familial and sub-familial levels leata, P. rubra, P. phosphorea, P. spinosum, V. mirabilis)
(Williams 1995; Dolan et al. 2013). Some of the families (Fig. 14.9). Cavernularia pusilla and V. cynomorium are
including Mediterranean deep-water species radially symmetrical while F. quadrangularis, K. stelliferum
(Kophobelemnidae, Pennatulidae and Protoptilidae) are and P. carpenteri are more or less bilateral. In P. aculeata, P.
polyphyletic. rubra, P. phosphorea and P. spinosum the polyp leaves are
146
Table 14.4 Some external features of the Mediterranean deep-sea pennatulaceans. Sizing refers to Mediterranean specimens (mainly according to Gili and Pagès 1987) and do not refer to maximal
sizes
Sclerites in the Calyces in
Colony shape/size Autozooids N° autozooids tentacles of the autozooids/n°
Species in cm Symmetry fusion/leaves on each leaf autozooids terminal teeth Mesozooids Siphonozooids Remarks
Family
Funiculinidae
Funiculina Thin, long, Bilateral Free – Absent Yes, spiculiferous/8 Absent Sparsely distributed Occurrence of
quadrangularis whip-like/145 (P) between autozooids three-flanged
sclerites
Family
Kophobelemnidae
Kophobelemnon Clavate/22 (P) Bilateral Free – Yes Absent Absent Numerous all over the Occurrence of
stelliferum rachis three-flanged
sclerites
Family
Pennatulidae
Pennatula aculeata Feather-like/24 Bilateral Fused/ ~15 Yes Yes, spiculiferous/8 Abundant in the Numerous in the Occurrence of
(P) leaves dorsal side of rachis, dorsal and ventral three-flanged
big-sized sides of rachis sclerites
Pennatula Feather-like/17 Bilateral Fused/ ~10 Yes Yes, spiculiferous/8 Absent? Numerous in the Occurrence of
phosphorea (P) leaves dorsal and ventral three-flanged
sides of rachis sclerites
Pennatula rubra Feather-like/20 Bilateral Fused/ ~50 Absent Yes, spiculiferous/4 Abundant in the Numerous in the Occurrence of
(P) leaves dorsal side of rachis; dorsal and ventral three-flanged
one on the base of the sides of rachis sclerites
leaves
Pteroeides Feather-like/12 Bilateral Fused/ ~100 Absent Yes, fleshy Absent Only in a proximal
spinosum (P) leaves zone of each polyp
leaf
Family
Protoptilidae
Protoptilum Long, slender/45 Bilateral Free – Yes Yes, spiculiferous/ Absent Numerous all over the Occurrence of
carpenteri (P) teeth no evident rachis three-flanged
sclerites
Family Veretillidae
Cavernularia Cylindrical to Radial Free – Absent Absent Absent Numerous all over the Autozooids fully
pusilla slightly clavate/~8 rachis retractile into rachis
(P)
Veretillum Cylindrical/50 (L) Radial Free – Absent Absent Absent Numerous all over the Autozooids fully
cynomorium rachis retractile into rachis
Family
Virgulariidae
Virgularia mirabilis Feather-like/35 Bilateral Fused/ ~16 Absent Yes, fleshy Absent Only in a single row at Colonies without
(P) leaves the foot of each leaf sclerites
A. Altuna and A. Poliseno
In some species, the size changes notably between live (L) and preserved (P) specimens. We refer to Kükenthal (1915) and Gili and Pagès (1987) for a full description and iconography of the species
well-developed and big-sized, giving a feather-like appear- uncommon and difficult, similarly studies on population
ance to the colony (Figs. 14.9 and 14.10), while in V. mirabi- density may be sometimes underestimated due to the ability
lis they are short and the feather appearance is less of some species to withdraw below the sediments surface.
pronounced. This capability has been noticed in K. stelliferum, V. mirabi-
Species identification among North-eastern Atlantic and lis, P. phosphorea and P. aculeata (Langton et al. 1990;
Mediterranean Pennatula has been problematic. However, Hughes 1998; De Clippele et al. 2015). In situ observations
the three Mediterranean species can be differentiated by the on withdrawal behavior of V. mirabilis were reported in
number of autozooids on each leaf and their orientation (see Mediterranean waters at 100 m depth (Ambroso et al. 2013).
Chimienti et al. 2015), occurrence of mesozooids associated Funiculina quadrangularis and P. phosphorea are near-
to the base of the leaves, number of teeth in the calyces, and cosmopolitan, a unique feature among the Mediterranean
presence of sclerites in the tentacles of the autozooids octocorals. Concerning P. phosphorea, several morphotypes
(Fig. 14.9, Table 14.4). Several P. phosphorea morphotypes and subspecies, in need of genetic corroborations, have been
were formerly described based on their colour differences described worldwide. Additionally, F. quadrangularis and P.
(see Kükenthal 1915). Cream-coloured specimens of P. carpenteri have rather wide bathymetric ranges, an uncom-
phosphorea and P. rubra co-occur at the same stations in the mon feature among octocorals. Funiculina quadrangularis is
Alborán Sea off Spain (Fig. 14.9a–e). Hence, chromatic vari- very sensitive to bottom fishing activities, as it shares habitat
ation in these species is of little value for taxonomic with important commercial crustaceans in the Mediterranean
determinations. Sea. Facies of this species have almost completely disap-
Kükenthal and Broch (1911) and Kükenthal (1915) pro- peared from the Mediterranean Sea (Sardà et al. 2004) so that
vided descriptions of the Mediterranean species. Further it has been categorised as “vulnerable” in the UICN red list
taxonomic and biological information on the Adriatic and (Otero et al. 2017; Otero and Marin, this volume).
North-western Mediterranean (off Catalonia) species were
published by Pax and Müller (1962), and Gili and Pagès Remarkable Sites and Distribution
(1987), respectively. Protoptilum carpenteri was thoroughly The most widely distributed species is F. quadrangularis,
described by Mastrototaro et al. (2014), whereas C. pusilla, followed by V. cynomorium, P. phosphorea and P. spinosum
P. rubra and P. spinosum were re-described by Abdelsalam (Vafidis 2010). Pennatula phosphorea and P. rubra are wide-
(2014) by considering shallow-water colonies collected off spread and abundant along the Mediterranean shelf, occur-
Egypt. The sea-pen sizes vary dramatically when colonies ring from the Sea of Marmara (Topçu and Öztürk 2015) to
are inflated, with remarkable differences among species the Alborán Sea (López-González 1993). On the contrary, P.
(Figs. 14.9 and 14.10). For example, colonies of V. cynomo- aculeata is a North Atlantic species known in the
rium measuring 50 cm in height are only 20 cm when pre- Mediterranean basin only from a few records along the
served (López-González 1993). Funiculina quadrangularis French coast (Thomson 1927) and in the Alborán Sea (Ocaña
is certainly the Mediterranean pennatulacean with the largest et al. 2000a) (Fig. 14.9f). Protoptilum carpenteri is known in
colony. Pax and Müller (1962) found Adriatic specimens the Ionian Sea and the Balearic Islands (Mastrototaro et al.
with colonies that may reach up to 145 cm in height 2014, 2017). Cavernularia pusilla is also uncommon; in
(Fig. 14.10a). Cavernularia pusilla is the smallest, reaching deep-waters occurs in the western basin and the Aegean Sea.
~6.0 cm in height when contracted (see Table 14.4). Overall, Kophobelemnon stelliferum is locally abundant in the west-
Mediterranean sea-pens do not reach sizes as high as those ern basin (Pardo et al. 2011; Bo et al. 2012a (as K. leuckar-
described from northern Europe such as for instance P. phos- tii); Mastrototaro et al. 2013), the Ionian basin (Vafidis et al.
phorea (40 cm) or F. quadrangularis (200 cm) (see Hughes 1994) and the Sea of Marmara (Topçu and Öztürk 2015, as
1998). Mediterranean small-sized specimens of K. stel- K. leuckartii). The highest species richness occurs in the
liferum collected by Mastrototaro et al. (2013) were attrib- western basin with ten species known after updating Vafidis
uted to possible “dwarfism” due to local hydrological (2010). Distribution maps of the deep-sea habitat forming
conditions. species F. quadrangularis and K. stelliferum are provided in
Protoptilum carpenteri is the unique species living only other chapters of this book (see Chimienti et al., this
deeper than 200 m depth. All others live in both coastal and volume).
deep off-shore areas (C. pusilla, F. quadrangularis, K. stel-
liferum, P. aculeata, P. phosphorea, P. rubra, P. spinosum, V.
cynomorium, V. mirabilis) (Table 14.2). Funiculina quadran- 14.3.3 Class Hydrozoa, Subclass Hydroidolina
gularis, K. stelliferum and P. aculeata are, however, of pre-
dominantly bathyal occurrence. Except for P. aculeata, an Hydrozoa is a group of mostly colonial cnidarians, frequently
uncommon species, Mediterranean Pennatulidae are mainly polymorphic, with sessile polyps and free-living medusae.
platform-inhabiting sea pens. Population assessments are They have tetramerous or polymerous radial s ymmetry, and
lack stomodeum (actynopharynx) (Hyman 1940). Polyps do Mediterranean Species

not have mesenteries, and the gastrovascular cavity is undi- Despite the abundance of anthoathecate hydroids in the
vided. Medusae, if present, are budded from the polyps and Mediterranean Sea with 142 species so far known (Boero
have a velum. The subclass Hydroidolina includes three and Bouillon 1993), only E. aspera is a CWC. This hydro-
orders, among which only the Anthoathecata includes coral was first discovered in the Mediterranean Sea and re-
Mediterranean CWCs as defined herein. However, some spe- described by Zibrowius and Cairns (1992), who gave a
cies in the order Leptothecata lacking calcareous skeletons, as comprehensive account with a review of the literature, ecol-
Lytocarpia spp., Nemertesia spp. and others, may attain large ogy and SEM images. Errina aspera forms white and porous
sizes and be important as habitat-forming species. We refer to calcareous colonies that grow up to ~20 cm and can ramify
Bouillon et al. (2006) for a full account of the class, and to either in a plane or building bush-like colonies with cylindri-
Bouillon et al. (2004) for the Mediterranean species. cal branches tapering to pointed tips (see Zibrowius and
Cairns 1992; Salvati et al. 2010; see Fig. 19.1 in Chimienti
14.3.3.1 Order Anthoathecata et al., this volume).
This order comprises hydroids without a perisarcal theca cov- In the North-east Atlantic there are 19 species and three
ering the hydranth body, and having medusae with gonads subspecies (Zibrowius and Cairns 1992), a considerable
confined on manubrium; medusae lack statocysts (Bouillon amount if compared with the Mediterranean basin. A possi-
et al. 2006). They are divided into two suborders, Filifera ble explanation to the lack of diversity within the
(hydranths with filiform tentacles) and Capitata (hydranths Mediterranean Sea might be the definitely insular distribu-
mostly with capitate tentacles). Only Stylasteridae (Filifera) tion of stylasterids, which are mainly found off small volca-
is represented in the Mediterranean by a unique species nic oceanic islands, archipelagos and seamounts (Cairns
(Errina aspera, see Fig. 19.1 in Chimienti et al., this volume). 1992). In this respect, no stylasterids were recorded from
Stylasterids frequently form a white or pigmented fan-shaped, “Erathostenes” Seamount in the Eastern Mediterranean
erect and rigid corallum of calcium carbonate, although basin (see Galil and Zibrowius 1992).
encrusting species occur as well. Polyps are polymorphic, Prosobranch gastropods of the genus Pedicularia are obli-
and include gastrozooids, dactylozooids and gonophores, gate symbionts of stylasterids. Hence, their occurrence in the
with the latter developed inside typical cup-like structures deep-sea or in the fossil record is considered an evidence for
known as ampullae. Stylasteridae are azooxanthellate and are the existence of stylasterids. Indeed, E. aspera is regularly
typically deep-sea organisms. It is a speciose family with found with traces of Pedicularia throughout its geographical
about 320 extant species (Cairns and Schuchert 2010). range (Zibrowius and Cairns 1992; Salvati et al. 2010).
Taxonomy and Taxonomic Characters Remarkable Sites and Distribution

The calcareous skeleton of stylasterids and its different com- Errina aspera is not widely distributed in the Mediterranean
ponents (e.g., cyclosystems, gastropores, dactylopores, Sea and its presence is limited to the Straits of Messina and
ampullae, gastrostyles, etc.) are commonly used in systemat- Gibraltar (Zibrowius and Cairns 1992; Giacobbe 2001;
ics to discriminate the different genera and species (see Giacobbe et al. 2007; Salvati et al. 2010; Chimienti et al.,
Zibrowius and Cairns 1992). this volume). Both areas can be considered of special interest
A paper on stylasterids anatomy is due to Moseley (1879), by the exceptional occurrence of this species, its abundance
while Cairns (2011) provided a detailed anatomical glossary and the environmental conditions. There are strong currents
of the family. An identification key of the North-eastern that seem to be important for the occurrence of this species
Atlantic and Mediterranean genera, including descriptions and its growth. A thorough study of the Messina population,
and SEM images of all species, was given by Zibrowius and occurring at 83–230 m depth, has been undertaken by Salvati
Cairns (1992). et al. (2010). In the Gibraltar area the same species occurs at
61–443 m depth (Álvarez-Pérez et al. 2005).
Molecular Aspects
A first morphology-based phylogenetic study of the stylaste-
rid genera was based on the skeletal features (Cairns 1984, 14.4 Overview
2011). These characters are also useful for species identifica-
tion. Genetic studies on stylasterids are limited compared to 14.4.1 Overall Biodiversity
other groups of hydroids in which, due to variability in taxo-
nomic characters, scientists are searching alternative identifi- The study of the Mediterranean deep-sea coral fauna started
cation schemes. A relatively recent phylogenetic study based long time ago and at least 47 of the species considered herein
on nuclear rRNA genes is now available (Lindner et al. 2008) were first described from the Mediterranean basin
and further studies are ongoing (see e.g., Cairns 2015). To (Table 14.2). The presence of important research laboratories,
date, there are no data published on E. aspera. some of them founded in the nineteenth century (e.g.,
Stazione Zoologica “Anton Dohrn” di Napoli), was essential (9%) and ten, among which the majority is represented by
for the exploration of the Mediterranean fauna and its diver- alcyonaceans (seven species), live only deeper than 200 m
sity. The biodiversity of these organisms in the Mediterranean depth (Table 14.2). This represents the 17.5% of all deep-sea
is unequal, with the western basin being better explored than Mediterranean alcyonaceans so far inventoried (40 species).
others. Overall, the western basin displays the highest diver- Comparisons with Atlantic areas as the Bay of Biscay (see
sity in terms of species richness. The expected biodiversity Altuna 2015) gives opposite results, as 77% of the 73 deep-
of the Mediterranean deep-sea corals and CWCs is difficult sea alcyonacea inventoried live only deeper than 200 m depth.
to predict. Our knowledge is restricted to few sites, mostly Although biased by the differences in sampling efforts,
from the western basin, and the unexplored areas are numer- the Mediterranean deep-sea fauna diversity is lower if com-
ous. Despite numerous recent expeditions to new promising pared with the North-east Atlantic one. In this respect,
locales, very little has been added to the inventories over the Grasshoff (1989) concluded that none of several characteris-
last years. In this context, further studies are needed, espe- tic Atlantic bathyal species of antipatharians, “gorgonians”
cially on the deep-water hard-bottom communities around and sea-pens cross the Gibraltar strait and live in the
canyons and seamounts, and the white coral frameworks. Mediterranean Sea. Species, genera or families typically
The Mediterranean fauna includes 82 species, among which observed in bathyal zones off the Iberian Peninsula, the
68 are colonial (83%), and 14 solitary (17%). All the solitary Iberian-Moroccan gulf and/or North-western Africa are
species are scleractinians. Thirteen deep-sea corals are con- absent from the Mediterranean Sea. This is remarkable in
sidered CWCs by their habitat-building ability at bathyal some taxa, as for instance, the Calcaxonia. Some chrysogor-
depths (16%). giids are abundant in the Gulf of Cadiz (Radicipes challeng-
The use of ROVs is allowing the discovery of exceptional eri), but members of the family are absent from the
sites and near-pristine CWC communities (e.g., Bo et al. Mediterranean Sea. Families Primnoidae (five genera and
2015). CWCs that were considered until now very rare or seven species known off the Atlantic coast of the Iberian
nearly extinct were repeatedly found and the geographic dis- Peninsula) and Isididae (five genera and six species) are rep-
tribution and bathymetric ranges of other species were resented by three genera and four species in the Mediterranean
recently reconsidered (see Mastrototaro et al. 2010; Bo et al. Sea. Similar examples have been reported in several taxa
2012a, 2015; Giusti et al. 2015; Chimienti et al., this vol- namely, Antipatharia, Octocorallia, Scleractinia and
ume). Despite all these efforts, there are no new records Stylasteridae.
since the early twentieth century for Antipatharia, the eigh- Concerning the order Scleractinia, Zibrowius (1980) con-
teenth century for Stylasteridae, and since the early nine- sidered the Mediterranean deep-sea fauna poor if compared
teenth century for Zoantharia (Table 14.2). As for with the Atlantic areas at the same latitudes. In this respect,
scleractinians, only Anomocora fecunda (Pardo et al. 2011) 30 species have been identified from a single seamount off
and dead colonies of Schyzocyathus fissilis (Taviani et al. North-western Spain (Galicia Bank, unpublished) at a depth
2011) have been discovered since Zibrowius (1980). interval ranging from 614 to 1764 m. Thirty species are a
Octocorals are an exception to some extent (see Table 14.2). considerable amount if compared with the only nine species
New findings within pennatulaceans are restricted to collected in the whole Mediterranean basin at depths greater
Protoptilum carpenteri, that was recorded for the first time than 600 m mostly inhabiting hard bottoms (Table 14.2). On
by Mastrototaro et al. (2015). As for Alcyonacea, new spe- the contrary, in the Galicia bank there is a similar number of
cies or records are more common since the late twentieth species that inhabit hard- (16 species) and soft-bottoms (14
century. For instance, new species were described by Carpine species). These differences are partially explained by the
and Grasshoff (1975, Placogorgia coronata, P. massiliensis, absence in the Mediterranean Sea of corals that prefer soft-
Spinimuricea klavereni), Weinberg (1986, Clavularia car- bottoms such as the scleractinian genera Deltocyathus,
pediem), López-González and Cunha (2010, Dendrobrachia Eguchipsammia, Flabellum, Fungiacyathus, Premocyathus
bonsai), and López-González et al. (2014, Chironephthya or Stephanocyathus, as well as the lack of some free-living
mediterranea). New records, even of previously unrecorded Caryophyllia species. We do not known in our present state
genera, are Acanella arbuscula, Acanthogorgia armata, of knowledge if the absence of these species is due to a lack
Anthomastus sp., Filigorgia guineensis, Nicella granifera of studies in certain environments, or if they actually do not
and Telestula septentrionalis. Most of these new records cor- inhabit the Mediterranean Sea. Reductions of species diver-
respond to the Alborán Sea and have been done during the sity compared to the nearby Atlantic areas are not compen-
twenty-first century. sated by a substantial increase in the Mediterranean
Despite having an average depth of 2500 m, with a maxi- endemics, as these are ~14% of the total deep-sea coral fauna
mum of 5121 m and the bathyal domain covering 60% of its (including near-endemic species). There are no endemic spe-
surface (WWF/IUCN 2004), no Mediterranean corals have cies restricted to depths greater than 200 m (Table 14.2).
been collected as deep as in the nearby Atlantic areas. Only The reasons explaining such a difference in species rich-
nine species have been recorded deeper than 1000 m depth ness between Mediterranean and nearby Atlantic faunas are
surely varied and have been discussed in other chapters of paramount. Moreover, the management of concrete conser-
this book. Apart from scleractinians (see chapters from the vation and protection strategies is not properly doable if our
“Past” section in this volume), the fossil records of deep-sea knowledge is altered or scarce. For this reason, inventories
corals are scarce and extremely rare. However, some fossil and studies on the CWCs communities are of great impor-
remains showed that several species and/or genera occurred tance, especially in the areas that are constantly subject to
in the Mediterranean Sea during the Pliocene (5.33–2.58 Ma) human impacts like the Mediterranean Sea. Although neces-
and Pleistocene (2.58–0.01 Ma) as documented for sary to monitorise future changes in the biota due to different
Enallopsammia, Flabellum, Fungiacyathus and factors, comprehensive biodiversity investigations of the
Stephanocyathus (Zibrowius and Placella 1982; Di Geronimo Mediterranean deep-sea corals are at the present state com-
et al. 2005; Vertino et al. 2014). Fossils of stylasterids in plicated and poor. The work to be done is notable and it
Europe and in the Mediterranean basin are rare (Zibrowius requires additional sampling efforts from under-investigated
and Cairns 1992). Nevertheless, a rich and exceptional upper and unknown areas as well as the revision of large museum
bathyal hard ground fauna including stylasterids was discov- collections and (re)description of species under modern stan-
ered in Carboneras (Almería, South-eastern Spain) (Barrier dards. Re-descriptions of type material, or the selection of
et al. 1991). This unique place, dated back to the Late neotypes for those species whose types were lost, is essen-
Miocene, included well-preserved fossils of at least eight tial. An example on this respect is the recovery of good spe-
genera (Calyptopora, Conopora, Crypthelia, Distichopora, cies such as Nidalia studeri or Daniela koreni described by
Lepidopora, Pliobothrus, Stenohelia, and Stylaster) and 14 von Koch (1891) (see López-González et al. 2012) that were
species. Interestingly, none of these genera occur now in the later forgotten. The material of the latter discovered by
Mediterranean as E. aspera is the only stylasterid described López-González et al. (2012) is pending re-description, and
from the whole basin. Finally, fossils of two species of once cleared it could confirm the exceptional occurrence of
Keratoisis (Isididae), a typical bathyal octocoral genus now the family Nephtheidae in the Mediterranean Sea. These
absent from the Mediterranean Sea, were found in Late cases are surely not unique, especially among octocorals,
Miocene, Pliocene and Late Pleistocene deposits from sev- and the study of old collections using new comparative mate-
eral Mediterranean areas (Grasshoff 1980; Barrier et al. rial will probably induce changes in the inventories of the
1991; Taviani et al. 2011). Mediterranean coral fauna so far known (see for instance the
examples of Acanella furcata and A. arbuscula, Saucier et al.
2017). It is however surprising that, despite relevant discov-
14.4.2 Future Perspectives eries of new areas with rich CWCs communities, the addi-
tions of new species and records is limited as already
Perspectives on the study and conservation of Mediterranean discussed. Whether this is due to a poor Mediterranean deep-
deep-sea corals and CWCs are overall optimistic. Scientists sea fauna compared with the nearby Atlantic areas, or to a
are now aware of their importance, and our knowledge on the lack of sampling, will be cleared in the forthcoming years
subject is rapidly increasing thank to technological advances. whenever new studies using molecular tools, and morpho-
One of the most important challenges will be to find a bal- logical descriptions of forgotten species will become
ance between resources exploitation and conservation (see available.
Otero and Marin, this volume), aiming to better protect the The use of molecular tools and the sequencing of DNA
environments and their biodiversity. Local communities and traits has revolutioned the systematics of cnidarians, contrib-
industries will compromise the financial benefits that marine uting sometimes to better investigate the relationships
resources can ensure. However, they should be aware that between different species rich taxa. Nevertheless, in some
they could also be guaranteed by policies of conservation groups, among which significant Mediterranean taxa of the
and protection of the species and their habitats. Several spe- family Plexauridae, the molecular markers used failed to dis-
cies are habitat-forming and can be often exploited by other criminate morphological puzzling species of genera such as
organisms due to their commercial interest, refuge, nurseries Paramuricea and Swiftia, or among and within genera like
or feeding purposes (see D’Onghia, this volume; Otero and Placogorgia and Paramuricea. Although cryptic biodiversity
Marin, this volume; Rueda et al., this volume). Deep-sea cor- can be suspected in some taxa, we do not always have tools
als and CWCs are mostly slow-growing organisms (see to detect it. Finally, and given that many Mediterranean spe-
Bramanti et al., this volume; Lartaud et al., this volume), cies were first described long time ago and that their types
some of them can even represent the most long-lived organ- went lost or are currently useless for genetic analyses, the
isms on the planet, but can be irreversibly damaged by rough challenge to link newly collected material to museum speci-
fishing practices (Bo et al. 2015; Otero and Marin, this vol- mens is obvious. In future a better knowledge of the
ume). This said, understanding the importance of these Mediterranean deep-sea coral fauna will require cooperation
organisms, their biodiversity, and community structure is between experts in different scientific disciplines.
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Habitat Mapping of Cold-Water Corals
in the Mediterranean Sea 15
Claudio Lo Iacono, Alessandra Savini,
Veerle A. I. Huvenne, and Eulàlia Gràcia
Abstract like structures (up to 300 m wide and 25 m high) associated
Habitat mapping is increasingly considered as a reliable with mass wasting events. Both cases adopt a holistic and
and efficient methodology to explore and represent the integrated study of the environmental characteristics
complexity and extent of benthic communities. Providing (geology and oceanography) of the observed benthic hab-
a full-coverage spatial perspective of habitat heterogene- itats and aim to map their extent using supervised auto-
ity is becoming an essential tool in science-based man- mated classifications. Multibeam swath bathymetry, the
agement of natural resources, specifically regarding derived acoustic backscatter, sidescan sonar, video foot-
vulnerable marine ecosystems such as cold-water corals. age gathered with a remotely operated vehicle, photo
Here we present two case studies, where we revisit known stills from underwater drop camera, and CTD casts where
cold-water coral areas of the Mediterranean Sea and available, have been used together to identify the geologi-
where we apply original habitat mapping techniques. The cal and oceanographic processes that most likely are
areas correspond to the Chella Bank, in the Alborán Sea, responsible for the distribution of the observed cold-water
and the Santa Maria de Leuca cold-water coral province, corals and associated benthic communities.
in the Ionian Sea. The Chella Bank is one of a series of
volcanic banks and knolls located in the western Keywords
Mediterranean that have been described as geologic fea- Habitat mapping · Cold-water corals · Geomorphology ·
tures hosting vulnerable marine ecosystems. The cold- Benthic habitats · Mediterranean Sea
water coral province off Santa Maria de Leuca represents
one of the largest known occurrences of living reef-
forming cold-water coral species (i.e. Lophelia pertusa
and Madrepora oculata) in the Mediterranean Sea, where 15.1 Introduction
corals grow on the exposed summits and flanks of mound-
Mapping the distribution of benthic habitats using robust and
objective methodologies can support science-based monitor-
C. Lo Iacono (*)
National Oceanography Centre, University of Southampton
ing, management and protection of natural marine resources,
Waterfront Campus, Southampton, UK specifically for deep-sea vulnerable marine ecosystems
Spanish National Research Council, Marine Sciences Institute,
(VMEs), whose dynamics are not entirely understood
Barcelona, Spain (European Parliament 2008; Farmer et al. 2012; Golon 2014;
e-mail: [email protected]; [email protected] Grehan et al. 2017). Habitat mapping aims to describe the
A. Savini distribution of seafloor habitats by exploring the interactions
Department of Earth and Environmental Sciences, University of between geological, ecological and oceanographic pro-
Milano-Bicocca, Milano, Italy cesses, allowing point data to be extended to full-coverage
V. A. I. Huvenne maps. Under this perspective, the application of geo-acoustic
Marine Geoscience – Seafloor Processes and Habitats Group, full-coverage mapping, supported by groundtruthing infor-
National Oceanography Centre, University of Southampton
Waterfront Campus, Southampton, UK
mation and water column measurements, gives additional
information to ecological studies by providing a realistic
E. Gràcia
Spanish National Research Council, Marine Sciences Institute,
view on the ecosystem structure and on its multi-scale spatial
Barcelona, Spain variability. The application of classical hull-mounted multi

https://doi.org/10.1007/978-3-319-91608-8_15
158 C. Lo Iacono et al.
Fig. 15.1 Schematic illustration displaying the different spatial scales approaches. Although both top-down and bottom-up classifications are
of the physical habitats associated with CWC ecosystems (sensu Green mostly associated with broad and fine spatial scales respectively, these
et al. 1999), the relative survey techniques (geo-acoustic and video) approaches can be applied over the full range of scales
applied in their exploration and the most adopted habitat mapping
beam (MB) systems and the increasing use of the most Seafloor acoustic backscatter (BS) is sensitive to the tex-
developed autonomous underwater vehicles (AUV) repre- tural properties (hardness and roughness) of the seafloor
sent the base for mapping and monitoring strategies of (Ferrini and Flood 2006; Lo Iacono et al. 2008; Brown et al.
marine environments at different spatial resolutions 2011; Pierdomenico et al. 2016). Acoustic BS can be used to
(Ramirez-Llodra et al. 2010; Wynn et al. 2014; Angeletti differentiate sedimentary facies associated with specific hab-
et al., this volume), spanning from large geo-habitats (e.g.: itats (Masson et al. 2003), to map seagrass distribution
continental shelves, submarine canyons, seamounts, scale of (Tonielli et al. 2016), to discern different degrees of biotur-
hundreds of meters to few kilometres) to small species bation as controlled by volume scattering (Urgelés et al.
assemblages (sub-metrical scale) (Fig. 15.1). 2002) or to distinguish living CWC colonies from coral rub-
As the distribution of species can be influenced by seabed ble (Huvenne et al. 2016). Nonetheless, despite full coverage
morphology (through substrate type and rugosity, fine-scale acoustic mapping being a key requirement, reliable maps of
effects of currents, distribution of food supply) MB swath benthic habitats need to be validated through ground-truth
bathymetry can provide digital terrain models (DTM) of the data (such as video, still photos or seafloor samples). Over
submarine landscape at resolutions which allow for the dif- recent years, further information from oceanographic data
ferentiation of physical boundaries between different benthic (bottom currents, wave regimes, tidal cycle, chemical prop-
habitats. Surrogates derived from DTMs (such as slope, erties of the water column etc..) are increasingly being inte-
aspect, bathymetric position index, rugosity) can then be grated with seafloor data to assess the interactions between
used as proxies to explain ecological patterns (Guinan et al. geological and oceanographic processes as driving mecha-
2000; Savini et al. 2014; Robert et al. 2016; Bargain et al. nisms for habitat distribution (Fabri et al. 2016), specifically
2017; Lastras et al., this volume; Angeletti et al., this vol- for passive filter-feeding organisms, which rely on food-rich
ume). This is specifically true for those environments dis- bottom currents (Roberts et al. 2009 and references therein).
playing a strong three dimensional (3D) complexity, as in the Habitat mapping techniques are progressively refined from
case of Mediterranean coralligenous build-ups (Lo Iacono subjective interpretations of habitat distributions to more
et al. 2018a) or framework forming scleractinian cold-water objective and time-saving approaches based on complex
corals (CWCs) (Freiwald et al. 2002; Savini and Corselli image analysis algorithms and statistical approaches, either
2010; Lo Iacono et al. 2014; Glogowski et al. 2015). Stony unsupervised or supervised.
CWCs can occur as isolated colonies or patchily distributed Habitat mapping and seafloor classification techniques
aggregations among a variety of different substrates, which can be broadly separated into two main approaches: top-
can only be captured by maps with sub-metrical resolutions down and bottom-up approaches (Brown et al. 2011;
(Davies et al. 2017). Under suitable environmental condi- Angeletti et al., this volume). Top-down habitat classifica-
tions alternating with less favourable conditions in a cyclical tions based on acoustic maps generally obtained through MB
pattern over time, CWCs are able to form reefs and mounds hull-mounted echo-sounders, have the advantage of covering
with a complex 3D structure. Mounds can reach a few hun- large areas, addressing the heterogeneity of geologic features
dreds of metres in height and can be several kilometres wide (mega-habitats sensu Green et al. 1999) as the main driving
(see a comprehensive list of references in Roberts et al. 2009; control in habitat distribution (LaFrance et al. 2014; Ismail
Lo Iacono et al. 2018a). et al. 2015). On the other hand, bottom-up approaches define
15 Habitat Mapping of Cold-Water Corals in the Mediterranean Sea 159
habitat boundaries based on the biological/ecological vari- phological and acoustic patterns associated with CWC com-
ability observed through punctual observations, and extrapo- munities, from mound to colony scale.
late/predict them on a broader scale by building statistical Here we present two case studies of habitat mapping of
relationships between biotic (e.g.: macrofaunal assemblages) Mediterranean areas containing CWC assemblages and asso-
and abiotic (geomorphology, sedimentary settings, water ciated species: the Chella Bank in the Alborán Sea (western
depth, water column etc.) characteristics of the environment Mediterranean) and the Santa Maria de Leuca (SML) CWC
(Fig. 15.1) (Davies et al. 2008; LaFrance et al. 2014; Robert province in the Ionian Sea (central Mediterranean). The
et al. 2015). areas are characterised and classified adopting similar
The ecosystems formed by CWCs, including stony corals, approaches, although at different spatial scales. Both regions
soft corals, black corals and gorgonians, are considered have already been described and recognised by national and
among the most endangered in the ocean (Freiwald et al. international organisations as physiographic features associ-
2004; UNGA 2006; Roberts et al. 2009; Otero and Marin, ated to a high level of biodiversity, with the occurrence of
this volume). Despite being aware of their relevant role in endangered VMEs, including CWC (de Juan and Lleonart
maintaining high levels of biodiversity in marine ecosys- 2010; OCEANA 2011, 2014; OCEANA and IEO 2014).
tems, the existence of these sensitive habitats is being seri-
ously compromised by anthropogenic activities, such as
commercial bottom trawling and ocean acidification (Reed 15.2 C
ASE STUDY 1 – The Chella Bank,
2002; Söffker et al. 2011; Baillon et al. 2012; Maier et al., Alborán Sea
this volume; Movilla, this volume; Otero and Marin, this vol-
ume). Their vulnerability to such massive impacts is making This case study revisits and implements previous observa-
scientific and political communities aware of the need for tions on the geomorphic features and benthic habitats of the
their conservation in several Exclusive Economic Zones Chella Bank, also named as “Seco de los Olivos”, in the NE
(EEZ) around the world. Thus, specific studies and dedicated Alborán Sea, and expands on those by integrating the pub-
measures to preserve natural resources are urgently needed, lished high-resolution swath bathymetry, BS data, and origi-
as well as detailed and statistically robust mapping method- nal video images and water column data (Fig. 15.2). The
ologies, and continued monitoring of the protected areas. Alborán Sea is located in the SW Mediterranean and dis-
Over the last few years, several studies have unveiled the plays several clusters of seamounts and volcanic banks host-
existence of living CWC communities in the Mediterranean ing VMEs (Milliman et al. 1972; Lo Iacono et al. 2008;
Sea (among others Taviani et al. 2005a; Schembri et al. 2007; Munòz et al. 2008; Oceana and IEO 2014; Palonimo et al.
Trincardi et al. 2007; Orejas et al. 2009; Vertino et al. 2010; 2015; Hebbeln, this volume; Wienberg, this volume;
Mastrototaro et al. 2010, 2017; Lo Iacono et al. 2012b; Palomino et al., this volume). Amongst those, the Chella
Cartes et al. 2013; Gori et al. 2013; Fabri et al. 2014; Bank is located in the northeastern sector of this basin within
Mytilineou et al. 2014; Taviani et al. 2017; Evans et al. 2016; a depth range of 70–700 m and is composed of middle
Fanelli et al. 2016; Grinyó et al. 2016; Aymà et al., this vol- Miocene to Pleistocene volcanic rocks (Duggen et al. 2004)
ume; Knittweis et al., this volume; Orejas et al., this vol- (Fig. 15.2). The Chella bank displays a sub-circular shape. It
ume). Nonetheless, the scientific understanding of the contains three main geomorphic features: a central sub-
dynamics and distribution patterns of CWC communities in horizontal flat top surrounded by two linear ridges at its
the Mediterranean is still far from complete. Despite the western and eastern sides (Coiras et al. 2010; Lo Iacono et al.
increasing availability of echosounders (hull mounted MB, 2012a), covering a total surface of up to 100 km2 (Fig. 15.2).
AUV mounted MB, SSS) and high-definition visual tools Previous studies in the area described the Chella Bank as a
(ROV and deep-towed cameras) within the European seamount hosting suitable habitats for CWCs, such as frame-
research fleets, relatively few studies adopted habitat map- work building corals and coral gardens (Lo Iacono et al.
ping approaches on CWC fields, trying to describe and quan- 2012a; OCEANA and IEO 2014). Data for this study com-
tify their extent and spatial patterns in a coherent way prise a high resolution bathymetric grid (10 m pixel size)
(Vertino et al. 2010; Lo Iacono et al. 2012b, 2014; de Juan acquired by the Instituto Español de Oceanografia (IEO)
et al. 2013; Fabri et al. 2014). Few habitat mapping studies using a Simrad EM300 hull-mounted MB echosounder
have used automated classification techniques, either (30 kHz, for further details see Coiras et al. 2010; Lo Iacono
attempting top-down (De Mol et al. 2012; Savini et al. 2014) et al. 2012a), a corresponding BS mosaic (5 m pixel size) and
or bottom-up approaches (Coiras et al. 2010; Vertino et al. videos/photos collected to ground-truth the seafloor. The
2010; Giusti et al. 2014; Lauria et al. 2015; Boavida et al. original videos/photos were acquired using a SeaTronic
2016; Fabri et al. 2016; Lo Iacono et al. 2018b). This is partly DTS6000 frame equipped with the HR camera Kongsberg
due to the lack of seafloor maps (MB and BS) whose spatial OE 14-208 and a small Mariscope-SPY ROV equipped with
resolution is high enough to allow the distinction of the mor- standard resolution cameras. Eleven CTD casts were
Fig. 15.2 (1) MB bathymetric map of the Chella Bank. The white lines vertical scale in m. (a) volcanic boulders and blocks with the glass
indicate the CTD transects carried out in the area, with dots indicating sponge Asconema setubalense, the black coral Antipathes dichotoma
the locations where the casts were acquired. The NW-SE oriented tran- and a small Dendrophyllia cornigera (class 5 in automatic classifica-
sect is displayed in (2); a, b, c and d indicate the locations where the tion); (b) coral garden including CWCs (class 1 in automatic classifica-
digital stills showed in the figure were taken. Blue lines indicate the tion); (c) dense and partly oxidised frameworks of dead Lophelia
ROV and digital camera transects used to ground-truth the area. The pertusa draped by fine grained sediments, with dense aggregations of
inset shows the location of the study area in the red circle. (2) Ophiothrix sp. observed on top of the CWC mound of the Chella Bank;
Backscatter mosaic acquired in the area. Light tones correspond to high (d) CWC frameworks and coral rubble with spotted gorgonians
BS values. The inset shows the chlorophyll fluorescence values acquired Acanthogorgia hirsuta observed along the flank of the CWC mound of
through the CTD casts along the NW-SE transect displayed in 1 (verti- the Chella Bank. The shark is an Oxynotus centrina. In this last photo,
cal black lines indicate the locations where the casts were acquired), the estimated inclination of the seafloor is between 14° and 18°
acquired on the Chella Bank with a Seabird SBE9 along two the EU-LIFE INDEMARES Project (OCEANA 2014;
transects crossing the centre of the Bank (Fig. 15.2-1). OCEANA and IEO 2014). Some of the species observed in
Turbidity, salinity, temperature, fluorescence and oxygen this area belong to the list of endangered species recognised
were recorded along the water column for each station. Video by different national and international conventions. The most
footage and CTD casts were acquired during the EVENT- relevant conventions which have been taken into consider-
SHELF and EVENT-DEEP Cruises, in the frame of the ation are: the Bonn Convention (Convention on the
EVENT Spanish National Project (CGl200612861-C02-02, Conservation of Migratory Species of Wild Animals), the EU
CTM2003.QJJ46-ElMAR). Habitats Directive (92/43/CEE), the Barcelona Convention
for the Protection of the Marine Environment and the Coastal
Region of the Mediterranean, the Mediterranean Red List of
15.2.1 Conservation Value of the Chella Bank endangered species produced by the International Union for
Conservation of Nature (IUCN) and the Spanish law 42/2007
The Chella Bank is one of the marine areas in Spanish waters for conservation of Natural Patrimony and Biodiversity.
designated as Sites of Community Importance (SCI) and Most of the vulnerable and endangered species belong to the
Special Areas of Conservation (SAC) under the EU Habitats Phyllum Cnidaria, which include CWC species such as
Directive. Evidence gathering was carried out in the frame of Antipathes dichotoma, Antipathella subpinnata, Savalia sav-
aglia (false black coral), Leiopathes glaberrima, disjunctions. The northern bank develops over a depth
Parantipathes larix, Lophelia pertusa, Madrepora oculata, range of 150–350 m and presents four main NW-SE trend-
Dendrophyllia cornigera, Dendrophyllia ramea, Eunicella ing ridges and a single NE-SW oriented ridge (Lo Iacono
verrucosa, Leptogorgia sarmentosa, Paramuricea clavata, et al. 2012a). Based on their morphology and on previous
Callogorgia verticillata. The Habitat 1170 (Reefs – Annex studies, these ridges are most likely composed of volcanic
I), identified based on the EU Habitats Directive (92/43/ rocks (Lo Iacono et al. 2012a; OCEANA and IEO 2014).
CEE), occurs on the Chella Bank. Based on video observa- Available video footage along the southern bank of the
tions, CWC communities show a poor conservation status eastern ridge suggests a low species richness and diversity
but with achievable actions towards their recovery and pres- along this sector, which is apparently dominated by scat-
ervation of a good environmental status (OCEANA and IEO tered specimens of the glass sponge A. setubalense.
2014). The Chella Bank has also been recognised as an area Contrasting with the geological nature and with the domi-
with relevant occurrence of cetaceans, such as Balaenoptera nant benthic communities of the two banks, original videos
acutorostrata, Delphinus delphis, Stenella coeruleoalba and and photo stills along the 2 km long sinuous feature con-
Globicephala melas, which are also described as endangered necting them has unveiled the biogenic origin of this relief.
species in Annex IV of the EU Habitats Directive (OCEANA Both the top and the flanks of this relief showed the pres-
2014; OCEANA and IEO 2014). ence of subfossil CWC frameworks (mainly L. pertusa and
D. cornigera). The top, at around 300 m deep, showed
dense frameworks of dead L. pertusa draped by a fine sedi-
15.2.2 The Chella Bank and Its Habitats ment veneer and intensely colonised by the brittlestar
Ophiothrix sp. Occasionally, scattered living colonies of M.
The western ridge of the Chella Bank extends for around oculata, D. cornigera, A. hirsuta, and the sponge P. monil-
16 km2 and covers a depth range of 160–620 m. (Fig. 15.2). ifera were registered. The flank displays a smooth morphol-
The ridge stretches in N-S direction in the southern half and ogy, consisting of dead L. pertusa frameworks and fine
bifurcates towards the north in a Northwest and a Northeast sediments showing an apparent stratification, spotted coral
direction (Fig. 15.2) (Lo Iacono et al. 2012a). The walls dis- rubble and bioclastic debris. Scattered specimens of the
play an average slope of 8°, with maximum values of 17°. gorgonian A. hirsuta and the black coral P. larix were reg-
Available data reveal the complex geological nature of peaks istered along the flank. Based on the available data, also
and crests along the ridge, which consist of hard and massive including seismic records crossing the area and imaging its
volcanic bedrock and volcanic breccias (Fig. 15.2a). More internal structure (Lo Iacono et al. 2011), the sinuous fea-
detailed information on the geology and geomorphology of ture along the Chella eastern ridge most probably corre-
the western ridge is available in Lo Iacono et al. (2012a). sponds to a CWC mound, up to 60 m tall. Similar cold-water
Original videos reveal that peaks and crests correspond to carbonate bioconstructions have already been described in
habitats mostly dominated by the hat-shaped glass sponge the same basin, south of the Chella Bank (Cabliers CWC
Asconema setubalense, accompanied by scattered stony cup mound: Lo Iacono et al. 2016, 2018a; East Melilla CWC
corals (D. cornigera), black corals (Anthipates sp.; Anthipates Mounds: Fink et al. 2013, Wienberg, this volume; West
dichotoma), gorgonians (Acanthogorgia hirsuta), grey Melilla CWC Mounds: Lo Iacono et al. 2014).
encrusting sponges (Hamacantha falcula) and sponges The top of the Chella Bank displays a sub-circular shape
(Pachastrella monilifera; Petrosia sp.). Sedimentary bottoms and covers a total surface of 7.6 km2 (Fig. 15.2). The area is
are mainly composed of muds mixed with fine sands, domi- composed of an irregular central sector showing a rough sea-
nated by different species of echinoids (Spatangus purpu- floor and a surrounding flat and sub-horizontal sector
reus, Cidaris cidaris, Echinus acutus), with scattered sea (Fig. 15.2). The irregular central sector ranges from 76 to
pens (Kophobelemnon stelliferum) and bamboo corals 118 m in depth and rises up from 5 up to 40 m above the sur-
(Isidella elongata). Coarse sand regions are randomly char- rounding bank top (Lo Iacono et al. 2012a). The BS image of
acterised by 40–50 cm long asymmetric ripples, suggesting this sector presents an alternation of high BS stripes corre-
the occurrence of unidirectional currents in the area (Lo lated to rocky outcrops in the video images, and low BS
Iacono et al. 2012a). facies where bioclastic coarse sandy sediments were
The eastern ridge of the Chella Bank covers a depth observed.
range of 100–480 m along a NW-SE trend and consists of The area surrounding the rough central sector presents a
two main banks connected by a linear, slightly sinuous smooth, low reflective sub-horizontal seafloor, with depths
2 km long and 400 m wide structure, 300 m deep and up to ranging from 130 to 115 m. In this area, the predominant
60 m high (Fig. 15.2) (Lo Iacono et al. 2012a). The south- seafloor substrate corresponds to coarse sands and gravels,
ern bank is a 200 m high sub-conical massif with slopes entirely composed of bioclasts (Fig. 15.2) (Lo Iacono et al.
from 15° to 20°. Based on video images, the southern bank 2012a). Analysis of the composition of the sands revealed
consists of basaltic slabs, in some cases showing typical the presence of planktonic foraminifera, shells, molluscs
(especially bivalves), echinoid spines and bryozoan remains –– Slope map, calculated from the above smoothed bathym-
(Lo Iacono et al. 2012a). etry (using ArcGIS)
Original video tracks along the rough rocky outcrops also –– Benthic Positioning Index map, calculated from the
revealed extensive fields of cemented bioclastic sediments smoothed bathymetry, using an annulus kernel with inner
mainly consisting of gravels and coarse sands. Based on radius of 8 pixels and outer radius of 21 pixels (using the
composition and depth of rocky outcrops, they likely corre- freely available Benthic Terrain Modeller 3.0 toolbox
spond to relict coastal deposits formed during previous sea (Wright et al. 2012).
level stages, and now provide substrate for a wide variety of –– Backscatter grid (10 m pixel), smoothed with a 5 × 5
gorgonians typically found along the Mediterranean shelf mean filter
edge and upper slope environments (Grinyó et al. 2016). –– Grey-Level Co-Occurrence Matrix (GLCM) Dissimilarity
Gorgonian species observed included C. verticillata, as defined by Haralick (1979), calculated in 21 × 21 pixel
Viminella flagellum, Swiftia pallida, P. clavata, Eunicella moving windows, with an inter-pixel distance of 8, aver-
cavolinii, E. verrucosa, Muriceides lepida and Ellisella aged over 4 directions and with backscatter reduced to 64
paraplexauroides. These gorgonian species form dense coral grey levels (in-house developed Matlab routine).
gardens that cover vast extents of the top of the Chella Bank. –– GLCM Entropy (Haralick 1979), calculated in 21 × 21
Among these gorgonian species, we also observed numerous pixel moving windows, with inter-pixel distance of 8,
colonies of the CWC D. cornigera, the recently described averaged over 4 directions and with backscatter reduced
soft coral Chironephthya mediterranea (López-González to 64 grey levels (Matlab).
et al. 2014), an undetermined species of the genus Alcyonium,
several large desmosponge species such as P. monilifera, Video and photography data were classified into the fol-
Aplysina cavernicola, Poecillastra compressa, Phakellia lowing dominant habitat types: (1) Rocky outcrops with
ventilabrum, the bryozoans Pentapora facialis, and the poly- coral gardens and gorgonian fields; (2) bioclastic coarse
chaete Salmacina disteri. Some gorgonian species presented sands and gravels with dominance of echinoids; (3) volcanic
substrate for large individuals of the epiphyte Astrospartus ridges with dominance of the glass sponge Asconema setub-
mediterraneus. Video tracks also showed that part of this alense and anthipatarians; (4) sub-outcropping volcanic
habitat has been seriously damaged by long-line fishing ridges draped by mud, with spotted glass sponge A. setub-
activities. alense; (5) fine bioclastic sediments; (6) CWC framework.
Processing of the acquired CTD casts shows increased The ROV video tracks were split into 200 m long sections
values of turbidity and fluorescence in the surface waters which, together with a series of point observations from the
overlying at the top of the Chella Bank (Fig. 15.2). The drop-camera, were selected as ground-truthing points. Every
observed increased values could arise from the interaction other 200 m section was discarded to limit the ‘spatial auto-
between the topography of the Bank and the circulation of correlation’ between samples. Twenty percent of the leftover
the highly productive surface waters, already described in sections/points of each class were randomly selected as test
the Alborán Sea (Uitz et al. 2012; Oguz et al. 2014). The samples to evaluate the classification. The other 80% were
acceleration of food-rich bottom currents, when interacting used to create “training areas”.
with the rough local topography, most likely represents the A Maximum Likelihood Classifier (MLC) algorithm was
driving mechanism controlling the occurrence of the used in ArcGIS to produce a full-coverage map for the rest of
observed extensive fields of CWC communities. Accelerated the Chella area. The result is presented in Fig. 15.3.
currents can increase the supply of particulate food and The automated classification was able to identify and map
induce the recruitment and growth of passive suspension out all six recognised substrate types. Our test dataset indi-
feeders, able to exploit suspended particles as a potential cated a very good performance: only one of the test samples
food source (Gili and Coma 1998). in the bioclastic sand class (2) was classified as fine sedi-
ments (5). Nonetheless, it is clear from Fig. 15.3 that the
noise in the MB and BS data also creates a number of mis-
15.2.3 Automatic Classification of Benthic classification patterns (generally recognisable because they
Habitats on the Chella Bank are oriented NS or EW). Moreover, the system showed a low
performance in isolating the distribution of the CWC frame-
The automated classification of the Chella Bank environ- work, which was erroneously found along the southern flank
ment was based on a combination of MB and BS data, of the seamount. The automated habitat classification already
together with still photos and videos for ground-truthing. produced in the same region by Coiras et al. (2010) came to
Input data to the classification process consisted of: broadly similar results, although limited to 3 instead of 6
classes. Coiras et al. 2010 used a linear classifier predicting
–– Bathymetry grid (10 m pixel), smoothed with a 3 × 3 the main habitat distribution on the Chella Bank employing
mean filter a Matlab’s classification routine for the three habitat classes
Fig. 15.3 Supervised automated classification of the benthic habitats glass sponge Asconema setubalense; Class 5: bioclastic fine sediments;
on the Chella Bank. Class 1: Coral gardens, found on top of the Bank; Class 6: dead CWC framework. See the text for a comprehensive
Class 2: bioclastic coarse sands and gravels, mainly found along the description of each class. Dots and lines represent the ground-truthing
outer sector of the top; Class 3: Volcanic ridges with dominance of the data (still photos and ROV tracks respectively). Different colours cor-
glass sponge Asconema setubalense and antipatharians; Class 4: sub- respond to the different assigned classes. Polygons represent the areas
outcropping volcanic rocks draped by muddy veneers, with spotted selected for the training and the control of the classification system
(flat seafloor with CWCs, hard substrates with sponges, including the summits of positive features associated to mass
sandy deposits) (for more details see Coiras et al. 2010). wasting geomorphologies. The province is located offshore
Despite a smaller number of adopted classes, results in the southern limit of the Apulian Peninsula, on the north-
Coiras et al. 2010 mainly coincide with what this study inde- eastern Ionian margin, along the Apulian plateau (Fig. 15.4).
pendently presents, giving confidence in the objective and The plateau is an antiform formed by a 6 km thick Mesozoic
repeatable aspect of our classification. carbonate platform, overlaid by a thin Plio-Quaternary sedi-
mentary succession which slightly thickens eastward
(Argnani et al. 2001). It is crosscut by a NNW-SSE normal
15.3 C
ASE STUDY 2 – The Santa Maria de fault network, which forms prominent fault scarps and prom-
Leuca CWC Province, Ionian Sea ontories towards the west. Late Pleistocene mass-wasting
deposits dominate instead the central/eastern sector of the
The CWC province off SML represents one of the largest surveyed plateau, shaping the seafloor in a number of land-
known occurrences of living scleractinian CWCs in the slide related landforms (headscarps, longitudinal and trans-
Mediterranean Sea, where dense aggregations of coral verse lineations, extensional and pressure ridges, sediment
topped mounds are distributed over more than 800 km2 on blocks, as described in Savini et al. 2016) (Fig. 15.4). As
the northern Ionian margin, between 500 and 1000 m in documented by the occurrence of sediment drifting (Taviani
depth (Savini et al. 2016; Chimienti et al., this volume). The et al. 2005b; Savini and Corselli 2010), the benthic environ-
extent of SML CWC habitats has been estimated recently at ment is also impacted by bottom currents, generated by a
multiple spatial scales (Savini et al. 2014) and is summarised core of cold (12.92 °C), less saline (38.64 psu), and oxygen-
here. A more exhaustive explanation on the control that local ated water of Adriatic origin that moves in geostrophic bal-
geomorphic processes have in determining CWC distribu- ance along isobaths of 600–1000 m (Budillon et al. 2010).
tion and extent across the whole surveyed area is provided, Data for this study have been collected over the past
where corals are spread on different geological features, 10 years (Corselli 2010; Savini et al. 2014) and are com-
Fig. 15.4 Distribution of coral-topped mounds in the northern Ionian ony of Madrepora oculata and the sponge Poecillastra compressa
Sea (SML CWC province). Top-left panel: MB bathymetric map (adapted from Vertino et al. 2010 and Savini et al. 2016); (b) live planar
showing the location of MTDs (semi-transparent gray polygon). Top- colonies of Madrepora oculata (adapted from Savini et al. 2016); (c)
right panel: a detail of the multibeam bathymetric map (see the black detail of a live Lophelia pertusa colony, some tiny branches of
inset in the top-left panel for location) showing the distribution of sedi- Madrepora oculata are visible on the upper left corner (adapted from
ment blocks (black polygons) within the exposed, partially exposed and Savini et al. 2016); (d) large colony of the antipatharian Leiopathes
buried MTDs. The white polygon indicates the location of the SSS glaberrima colonising, together with scleractinians, dead coral frame-
mosaic of Fig. 15.5. Bottom panels include 4 representative Pluto- works and hardground crusts interspersed with mud (adapted from
ROV seafloor images of coral-dominated macro-habitats: (a) live col- Savini et al. 2016). Scale bar: 10 cm (a–c), 3 cm (d)
prised of a MB dataset (30 m pixel size) acquired through a 15.3.1 Conservation Value of the SML
hull-mounted Reson SeaBat 8160 (50 KHz), a Klein 3000 CWC Province
SSS backscatter mosaic for certain selected sites (1 m pixel
size) and videos/photos collected for ground-truthing using D’Onghia et al. (2017) presented recently a comprehensive
the Modus Gas Shipack deep-sea module (Etiope et al. 2010) resume of conservation value and incidence of anthropo-
equipped with cameras, or an observation class ROV – Pluto genic impacts on CWC habitats of the SML province. The
(Vertino et al. 2010) equipped with a HR camera. CTD casts province is included among the selected areas of conserva-
were acquired on the margin with a Seabird SBE9 along four tion interest in the open Mediterranean Sea, which includes
transects crossing the whole province from N to S, identifying the deep-sea (Specially Protected Areas of Mediterranean
the core of the Adriatic Deep Water (ADW) flow, associated Importance – SPAMIs) (UNEP-MAP RAC/SPA, UNEP-
with the CWC distribution (Budillon et al. 2010). Most of the MAP-RAC/SPA 2009, UNEP-MAP-RAC/SPA 2010,
data have been analysed in recent literature (Freiwald et al. UNEP-MAP-RAC/SPA 2011; de Juan et al. 2012). Based
2009; Corselli 2010; Savini et al. 2014; Bargain et al. 2017), on criteria of rarity, importance for life history stages of spe-
although for seafloor mapping data, published results are still cies, importance for threatened and endangered species/
fragmented and not presented in comparable forms. habitats, vulnerability, biological diversity and naturalness,
the SML CWC province is considered a “Vulnerable habi- rary extinction during the Early to Mid Holocene (from 11.4
tat” (de Juan and Lleonart 2010). In addition, this to 5.9 cal kyr BP), at the time of the sapropel S1 event, dur-
Mediterranean CWC area is also included among the pro- ing which the deep eastern Mediterranean basin turned
posed priority conservation areas suggested by several con- anoxic (Fink et al. 2012). Nonetheless present-day oceano-
servation initiatives (e.g. UNEP MAP EBSA; CIESM/ graphic conditions (Manca et al. 2006; Budillon et al. 2010)
Mediterranean Marine Peace Parks; Oceana/MedNet) coupled with an on-going uplift (Carminati and Doglioni
(Oceana 2011; Micheli et al. 2013). Taking into account the 2012) of the margin (which reduced the accommodation
documented impact of trawling and, to a lesser extent, of space promoting low sedimentation rate in most part of the
other types of fishing gear on the deep-sea coral community, exposed MTDs) represent the most important geo-environ-
the General Fisheries Commission for the Mediterranean mental controls that allow scleractinian corals to thrive on
(GFCM) created in January 2006 the new legal category of the upper and north-eastern slopes of a huge number of
“Fisheries Restricted Area” (FRA) at the SML CWC prov- exposed and partially exposed sediment blocks (Vertino
ince (D’Onghia et al. 2012; Otero and Marin, this volume). et al. 2010; Rosso et al. 2010; Savini et al. 2014, 2016).
Towed dredges and bottom trawl nets have been prohibited Nevertheless other settings seem to offer suitable areas for
in the FRA, which covers a part of the SML CWC province. coral growth on the margin. Freiwald et al. (2009) reported
Members are required to call the attention of the appropriate the occurrence of small-scale bioconstructions on the sub-
authorities in order to protect this FRA from the impacts of vertical and overhanging walls of a main canyon system,
any activity jeopardising the conservation of this spectacu- located to the west. Savini and Corselli (2010) also published
lar submerged landscape (GFCM-RAC/SPA GFCM-RAC/S mosaics of high frequency SSS data acquired along an ero-
2007), dotted by more than 1000 sub-conical and elongated sive and gently-sloping surface forming the western flank of
coral-topped mounds, located in water depths of 500–900 m. a prominent ridge that typifies the south-central sector of the
Unauthorised operations likely take place within the FRA, surveyed area, where coral colonies, along with hardground
even if trawling is formally illegal. Indeed, recent explora- facies, are patchily distributed as described in Rosso et al.
tions have provided images of trawl marks and solid waste (2010), without creating prominent geomorphological fea-
along the coral community (Freiwald et al. 2009; Vertino tures (i.e. mounds detectable on standard hull-mounted mul-
et al. 2010; Savini et al. 2014; D’Onghia et al. 2017), indi- tibeam bathymetry). An additional location to the west of the
cating that trawlers sometimes operate inside the northern coral occurrences has been also documented in Malinverno
limit of the FRA (Indennidate et al. 2010). et al. (2010) and Savini et al. (2014), associated to a series of
narrow ridges and fault scarps, where corals form extensive
framework at their top, here assuming a mound shape and
15.3.2 The SML CWC Topped Mounds producing typical hyperboles on seismic data.
and Other Coral Facies Detailed investigations on the overall biodiversity and
mapping activities were carried out only at those locations in
The SML CWC province was first mapped in 2004 (Savini which reef-forming species contributed in generating coral-
and Corselli 2010) and since then has become the focus of a topped mounds and identified respectively 222 species
series of oceanographic expeditions examining the overall (Mastrototaro et al. 2010) and a total of 13 distinct macro-
biodiversity of CWC habitats (D’Onghia et al. 2010; Rosso habitats (sensu Green et al. 1999). These include Lophelia
et al. 2010; Mastrototaro et al. 2010; Vertino et al. 2010; pertusa and Madrepora oculata coral frameworks, that pre-
D’Onghia, this volume) and the geological-stratigraphic vail on the summits and on the eastern mound flanks, and
framework in which corals grow (Malinverno et al. 2010). hardground crusts and boulders colonised by the antipathar-
The majority of research activities were carried out explor- ian species Leiopathes glaberrima (Vertino et al. 2010). A
ing some representative coral-topped mounds (Savini et al. fine scale macro-habitat characterisation and mapping is still
2016), located in water depths of 500–900 m, originally missing from the other areas.
formed as sediment blocks (originating from by late
Pleistocene Mass-Transport Deposits – MTDs) that likely
offered widespread suitable substrate for coral colonisation 15.3.3 Supervised Automatic Classification
during the last deglaciation (i.e.: 13.4–11.4 cal kyr BP, of SML Coral Facies
according to the oldest dated coral fragment reported in
Malinverno et al. (2010) and Fink et al. (2012)). Coral- Exploration by means of a 100–500 kHz SSS (Klein 3000)
topped mounds are sub-circular to elongated, 200 m wide in was performed in an operating range of 300 m at four main
average, from few meters to 25 m high and densely aggre- sites located between 400 and 700 m water depth. As
gated at places (i.e. more than 5 mounds per km2 – Fig. 16.2 in described in Savini et al. (2014), quantitative textural mea-
Savini et al. 2016). Analysis of sediment cores collected at surements were computed on the obtained SSS mosaics using
the top of sampled coral-topped mounds, revealed a tempo- co-occurrence matrices (Haralick 1973; Reed and Hussong
Fig. 15.5 The SSS mosaic (left – see Fig. 15.4 for location) and the rudstone and mud; (HgM) mudstone and mud; (MHc) mud and corals;
obtained classification map (right) representing the distribution of the (MHcr) mud and coral rudstone; (MHg) mud and mudstone; (M) mud;
six acoustic classes at MS06 site. Acronyms in brackets within the leg- (CrM) coral rubble and mud; (MCr) mud and coral rubble; (Cr) coral
end represent macrohabitats associated to each class: (Hc) coral frame- rubble; (Hg) Mudstone. (Detailed explanation are provided in Savini
work; (Hcr) coral rudstone; (HcM) corals and mud; (HcrM) coral et al. 2014)
1989; Gao et al. 1998; Huvenne et al. 2002; Savini 2004), of the provided DTM, at MS06 site (see Savini et al. 2014 for
using a similar approach as described previously for the further details). To the west, the second area is located at the
Chella Bank (see Savini et al. 2014 for further details) with top of a ridge (MS08), which enhances the step-like mor-
accuracy assessment performed according to Pontius and phology of the margin towards the west.
Millones (2011). Relying on the ground-truthing information At the MS06 site coral macrohabitats, with significant
obtained from sediment samples and visual investigations, a abundance of living coral frameworks (namely coral frame-
number of training areas were selected to represent six dis- works/rudstone described in Savini et al. 2014 and grouped
tinct acoustic classes, defined by coupling expert interpreta- in classes 1 and 2), dominate the mound’s tops and the north-
tion with results from the textural analysis (see Fig. 4 in eastern flanks. The western mound’s flanks are instead typi-
Savini et al. 2014). A Maximum Likelihood Classification fied by a mosaic of coral rubble, coral rudstone fragments
algorithm (according to Gibson and Power 2000) was subse- (from pebbles to boulders), dismantled hardground crusts
quently applied to generate a full-coverage classification map (resulting in clustered to isolated elements highly colonised
for each mosaic. Each class was then converted into polygons by solitary corals) and mud, with a high lateral variability in
(following integration of the classification maps in ArcGIS™) their distribution. Small scale parallel surface deformations
in order to quantify the total coverage for each of the defined originated by sediment thrusted south-westward are also vis-
acoustic facies, as indicated in Fig. 7 of Savini et al. (2014). ible in inter-mounds areas, where sedimentary facies domi-
As it was outside the scope of the Savini et al. (2014) nated by coral rubble or buried (at place partially) rubble
study, details regarding the spatial distribution of acoustic (occasionally hosting sparse coral colonies) were observed
facies at the different locations were not reported. We therein recoded videos (Vertino et al. 2010), generating coral
fore illustrate in Figs. 15.5 and 15.6 how the performed macrohabitats grouped in class 2. Worthy of attention on the
supervised automatic classification, showed the fine scale western mound’s flanks is the exclusive occurrence of
habitat distribution over two distinct areas (namely MS06 “Antipatharian Facies” described by Vertino et al. (2010) and
and MS08 as indicated in Fig. 15.4). The first area (Fig. 15.5) Rosso et al. (2010), consistently characterised by meter-
represents coral-topped mounds located in the central sector sized specimens of the black coral species L. glaberrima on
Fig. 15.6 The SSS mosaic (left – see Fig. 15.4 for location) and the rudstone and mud; (HgM) mudstone and mud; (MHc) mud and corals;
obtained classification map (right) representing the distribution of the (MHcr) mud and coral rudstone; (MHg) mud and mudstone; (M) mud;
six acoustic classes at MS08 site. Acronyms in brackets within the leg- (CrM) coral rubble and mud; (MCr) mud and coral rubble; (Cr) coral
end represent macrohabitats associated to each class: (Hc) coral frame- rubble; (Hg) Mudstone. (Detailed explanation are provided in Savini
work; (Hcr) coral rudstone; (HcM) corals and mud; (HcrM) coral et al. 2014)
a mixed seafloor. Distinctions between scleractinian domi- mounds in this area still remain largely unexplored and un-
nated facies and Antipatharian facies could not be achieved quantified. Future systematic research is thus needed to over-
based on the side scan sonar mosaic, although the latter were come the limitations of previous studies investigating how
consistently observed in those facies grouped under class 2. interactions between hydrography, topography and present-
At MS08, corals still formed mounds, although their ori- day sedimentary processes influence the assembly and struc-
gin is not related to mound-like sediment blocks displaced tural complexity of the reef-forming species present over the
by failure events. Mounds are located at the top of a ridge, whole SML CWC province.
where evidence from core samples, coupled with observa-
tions from shallow geophysics, testified to the presence of a
widespread erosional surface, leading to the emergence of 15.4 Conclusions
stiff/hardened substrata, constituted by older sediments dated
to the early to middle Pleistocene (Malinverno et al. 2010), The distribution patterns and spatial complexity of CWC com-
which likely offered suitable substratum for coral growth. munities and associated habitats have been revisited and
Few data from videos and samples are available to compre- described at two representative sites of the Mediterranean basin
hensively describe the variety of coral facies and especially through previously published geophysical data (MB bathymet-
their distribution pattern in this area. Nonetheless based on ric data and associated BS, SSS), interpreted with new water
the acoustic patterns recognized in classes 1 and 2 (coral column data (CTDs) and new ground-truth data (video, photos
dominated facies), the overall growth structure of coral facies and seafloor samples), and finally mapped and classified through
appears more homogenous over the gross mound morphol- the application of (supervised) automatic classification routines.
ogy, where coalescing coral reefs (as interpreted based on Our interpretations confirm that seafloor complexity, most
their acoustic response and video images) gave rise to CWC likely together with physical/chemical properties of the water
mounds (displaying a well defined mounded 3D structure column are two factors of crucial importance in driving the dis-
with sub-circular bases – Fig. 15.5), reaching dimensions of tribution and development of CWC communities.
up to few meters in height and from 100 to 200 m in diame- The produced habitat maps provide quantitative informa-
ter. The mechanisms promoting the formation of coral tion on estimated CWC extent and represent examples of
scientific products useful in supporting marine spatial plan- Brown CJ, Todd BJ, Kostylev VE, et al (2011) Image-based classifi-
cation of multibeam sonar backscatter data for objective surficial
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Cartes JE, Lo Iacono C, Mamouridis V, et al (2013) Geomorphological,
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An important strategic goal in habitat mapping regards gata assemblages in the deep Mediterranean: to what extent does
the definition of protocols and standardised methodologies Isidella form habitat for fish and invertebrates? Deep-Sea Res Part 1
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Acknowledgements The research on the Chella Bank benefited from 57:345–359
the Project EVENT (Integration of new technologies in paleoseismology: Davies AJ, Wisshak M, Orr JC, et al (2008) Predicting suitable habitat
Characterisation of faults capable to produce earthquakes and tsunamis in for the cold-water coral Lophelia pertusa (Scleractinia). Deep-Sea
south Iberia – CGl200612861-C02-02, CTM2003.QJJ46-ElMAR). We Res Part 1 Oceanogr Res Pap 55–8:1048–1062
acknowledge the helpful contribution of Jordi Grinyó (ICM-CSIC), Davies JS, Guillaumont B, Tempera F, et al (2017) A cold-water coral
which supported the species recognition on the Chella Bank. We deeply biota classification scheme for ecosystem-based management of the
thank the EVENT-Shelf and EVENT-DEEP Cruise parties, specifically deep sea. Deep-Sea Res Part 2 Top Stud Oceanogr 145:102–109
Rafael Bartolomé (ICM-CSIC) for contributing in the acquisition of D’Onghia G, Maiorano P, Sion L, et al (2010) Effects of deep-water
some of the video data. We are extremely grateful to Jose Ignacio Diaz coral banks on the abundance and size structure of the megafauna
and José Luis Sanz from the Spanish Institute of Oceanography (IEO) for in the Mediterranean Sea. Deep-Sea Res Part 2 Top Stud Oceanogr
having provided the multi beam and relative backscatter dataset of the 57:397–411
Chella Bank. We finally thank Montse Demestre (ICM-CSIC) and Xavier D’Onghia G, Maiorano P, Carlucci R, et al (2012) Comparing deep-sea
Monteys (GSI-Ireland) for providing the ROV and the digital still camera fish Fauna between coral and non-coral “megahabitats” in the Santa
used on the Chella Bank. Data for the study on the SML CWC province Maria di Leuca cold-water coral province (Mediterranean Sea).
were collected and analysed within the framework of the EU FP7 project PLoS One 7:e44509. https://doi.org/10.1371/journal.pone.0044509
CoralFish (Ecosystem-based management of corals, fish and fisheries in D’Onghia G, Calculli C, Capezzuto F, et al (2017) Anthropogenic
the deep waters of Europe and beyond, Grant agreement number: impact in the Santa Maria di Leuca cold-water coral province
213144 – www.eu-fp7-coralfish.net), the Italian project MAGIC (Mediterranean Sea): observations and conservation straits.
(Mapping Geohazard along the Italian Coasts – www.magicproject.it) Deep-Sea Res Part 2 Top Stud Oceanogr 145:87–101. https://doi.
and the FIRB program 2004/2006 RBAU 01RKC7_004 APLABES. The org/10.1016/j.dsr2.2016.02.012
research on the SML area also benefited from the EU FP6 project De Mol B, Amblas D, Calafat A, et al (2012) Cold-water coral colo-
HERMES (Hotspot Ecosystem Research on the Margins of European nization of Alboran Sea Knolls, Western Mediterranean Sea. In:
Seas, Contract number GOCE-CT-2005- 511234), the RITMARE project Harris P, Baker E (eds) Seafloor geomorphology as benthic habitat:
funded by the Italian Ministry of University and Research (MIUR) and GeoHab Atlas of seafloor geomorphic features and benthic habitats.
the ESF COCARDE Network. We are finally indebted to the two review- Elsevier, Amsterdam, Boston, pp 819–829
ers who have deeply improved the quality of this chapter with their con- de Juan S, Lleonart J (2010) A conceptual framework for the protec-
structive observations. tion of vulnerable habitats impacted by fishing activities in the
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Alborán Sea: from coral mounds and species dominance
com/5754
Cold-Water Coral Habitat Mapping
in the Mediterranean Sea: 16
Methodologies and Perspectives
Lorenzo Angeletti, Annaëlle Bargain, Elisabetta Campiani,

Federica Foglini, Valentina Grande, Elisa Leidi,
Alessandra Mercorella, Mariacristina Prampolini,
and Marco Taviani
Abstract Keywords
The marine scientific community developed new habitat Cold-water corals · Habitat mapping · Geophysical data ·
mapping procedures that proved to be effective to map Mediterranean Sea
seafloor habitats in a holistic manner, thus refining our
knowledge of benthic sea life. Several works on this
topic focused on cold-water coral habitats at the global 16.1 Introduction
scale, with focus on the Atlantic Ocean while, only a
few studies applied these methods to the Mediterranean Reliable description and classification of seafloor habitats
Sea. The prime objective of this chapter is to comment and their resident benthic life are needed for assessing man-
the methodologies used to describe cold-water coral agement and conservation measures, especially the impact of
habitats and map their extension; secondly we discuss growing anthropogenic pressures. Considering how little of
statistical models to outline the most suitable areas for the global seafloor has been mapped in comparison with ter-
cold-water coral settlement (habitat suitability models). restrial environments (Sandwell et al. 2006), there is an
Furthermore, recent technological developments in urgent need to collect and integrate spatial information
habitat mapping procedures provide geophysical data related to the distribution of marine biotic and abiotic com-
and seafloor images of higher resolution than ever ponents to effectively build benthic habitat maps (Kostylev
before, while multi- frequency systems supply new et al. 2001; Robert et al. 2016).
hyperspectral images of the seabed. This new type of Habitat mapping defies a simple and univocal definition
data could be crucial for a better characterisation of (e.g. Morris 2003; Mitchell 2005; Greene et al. 2007; MESH
such Mediterranean cnidarian habitats. Here we 2008a, b; Tillin et al. 2008; Costello 2009; Brown et al.
reviewed the procedures for the Mediterranean cold- 2011). A pragmatic definition was provided in 2008 as part
water coral habitat mapping applied so far, describing of the MESH (Mapping European Seabed Habitats) project;
two case studies in the Southern Adriatic Sea and dis- “Plotting the distribution and extent of habitats to create a
cussing caveats and future perspectives. map with complete coverage of the seabed showing distinct
boundaries separating adjacent habitats”. Despite the lack of
a standard definition, there is a consensus that a habitat can
be identified only through an integrated approach that mea-
sures, analyses and considers in full the physical, biological,
chemical and oceanographic aspects characterising that spe-
L. Angeletti · A. Bargain · E. Campiani · F. Foglini · V. Grande cific area on different spatial scales. To this end, different
E. Leidi · A. Mercorella · M. Prampolini (*) approaches and methods have been proposed (e.g. Greene
et al. 1999; Diaz et al. 2004; MESH 2008a, b; Brown et al.
2011; Lecours et al. 2015 and references therein). Acoustic
M. Taviani
technologies (multibeam echosounder, side scan sonar, etc.)
are used to acquire remote-sensing data of the seabed at a
large scale, while bottom samples, video footage and pho-
Woods Hole, MA, USA
tography provide information at fine scale. Hence, there is a

https://doi.org/10.1007/978-3-319-91608-8_16
Fig. 16.1 Schematic
overview of the
complementary approaches
usually applied for habitat
mapping. (Modified from
Brown et al. 2011)
large mismatch between the large and the very fine scale and CWC habitat mapping in the Mediterranean, and comment-
a major challenge in benthic habitat mapping is a consistent ing upon caveats and future perspectives. Our discussion will
integration of these two types of information (Brown et al. consider two case studies from the Southern Adriatic Sea, the
2011). Several strategies are used to obtain habitat maps Bari Canyon and the Montenegro slope (Fig. 16.2).
going from top-down to bottom-up approaches (Brown et al. Geophysical information on these sites is reported in
2011) (Fig. 16.1). Trincardi et al. (2007, 2014), Foglini et al. (2016a), and
There is a growing application of habitat mapping to the Angeletti et al. (2015a), while CWC presence is discussed by
exploration of cold-water coral (CWC) grounds, mainly Freiwald et al. (2009), Angeletti et al. (2014), and Taviani
focused upon the Atlantic Ocean (Davies et al. 2008; Dolan et al. (2011, 2016).
et al. 2008; Guinan et al. 2009a, b; Tong et al. 2012, 2013;
García-Alegre et al. 2014; Ross et al. 2017) and the
Mediterranean Sea (Lo Iacono et al. 2008, this volume; 16.2 Large Scale Data
Savini and Corselli 2010; Vertino et al. 2010, 2014; Savini
et al. 2014). The main concepts and operations related to 16.2.1 Bathymetric Data
CWC habitats mapping are presented by Lo Iacono et al.,
(this volume), with examples from the Ionian and Alborán The influence of seafloor bathymetry and morphology on the
seas. This chapter provides further discussion on this topic submarine environment, including oceanographic and sedi-
by examining critically the various methodologies applied to mentary patterns and type of biota, is well documented for
16 Cold-Water Coral Habitat Mapping in the Mediterranean: Methodologies 175
Fig. 16.2 Bathymetry of the

Southern Adriatic Sea
(EMODnet repository: http://
www.emodnet.eu/) and
geographic setting of the case
studies shown in this chapter:
Bari Canyon and Montenegro
continental slope
the Mediterranean Sea (Genin et al. 1986; Fredericksen et al. Position Index, Ruggedness, Terrain Surface Texture, Vector
1992; Canals et al. 2006; De Geest et al. 2008; Trincardi Ruggedness Measure, and many others. Geographic
et al. 2014; Bonaldo et al. 2016; Foglini et al. 2016a; Rebesco Information System (GIS) software usually offers tools to
and Taviani, this volume, with references). CWCs are gener- perform this task, unfortunately often using different algo-
ally thriving on hard substrates at depths between ca. 200 rithms for the same metric. Available software include
and 1000 m, characterised by strong bottom currents (e.g. GRASS, SAGA, Spatial Analyst toolset of ArcGIS, Benthic
Roberts et al. 2009). Thus, seafloor bathymetry and mor- Terrain Modeller (Wright et al. 2012), ArcGeomorphometry
phology are fundamental aspects to consider for identifying (Rigol-Sanchez et al. 2015), BSG seabed mapping toolbox
CWC sites and need to be included in habitat mapping and (De Clippele et al. 2016), TASSE (Terrain Attribute Selection
model predictions (Mortensen and Buhl-Mortensen 2004; for Spatial Ecology: Lecours et al. 2015, 2017) and other
Harris and Baker 2011; Lo Iacono et al. 2014, this volume; software (Wood 2009).
Robert et al. 2016; Fabri et al. 2017). Multibeam The slope is the first derivative of the bathymetric DEM
Echosounders (MBES) provide bathymetry and morphology and indicates the steepness of the terrain in degrees or in per-
data with continuous coverage and high-resolution (Roberts centage, while the aspect identifies the slope orientation with
et al. 2005; Durán-Muñoz et al. 2009; Correa et al. 2013; respect to the north and it is expressed in clockwise degrees
Savini et al. 2014; Lo Iacono et al., this volume). from 0 to 360 relative to North. Jointly, slope and aspect have
been used as an approximation of topographic exposure to
6.2.1.1 Terrain Morphometric Attributes
1 bottom current regimes (Davies et al. 2008; Edinger et al.
Seafloor morphology can be described quantitatively (geo- 2011). The curvature (plan and profile) is the second deriva-
morphometry: Lecours et al. 2016) through a number of met- tive and describes concavity and convexity of the slope,
rics that can be calculated from the Digital Elevation Model which influences the acceleration or deceleration of the cur-
(DEM), including slope, aspect, curvature, Bathymetric rents and thus provides information on erosional and deposi-
tional processes. The Bathymetric Position Index (BPI) gravelly beds), while low intensity values are typically
describes the relative elevation of an area with respect to its related to soft sediments, such as mud, clay, or fine sand
surroundings, thus identifying topographic highs, often (Hughes Clarke et al. 1997; Lurton and Lamarche 2015). By
related to bedrock outcrop and/or hard substrates (Wright giving qualitative indication on the type and quality of the
et al. 2012). Ruggedness, Terrain Surface Texture, Vector seafloor, backscatter data could then provide predictive
Ruggedness Measure are all measures of the terrain rough- information on resident biological communities or their
ness and can thus be used as a proxy for sediment and sub- activity (Urgelés et al. 2002; De Falco et al. 2010), including
strate type (Dunn and Halpin 2009). All of these measures CWC colonies, reefs or mounds (Fosså et al. 2005; Lo Iacono
can be calculated at different spatial scales, thus describing et al. 2008; Huvenne et al. 2005, 2016a, b). However, some
seafloor morphology at several scales (Wilson et al. 2007). ambiguities on a direct correspondence between acoustic
They have been widely used in CWC habitat mapping and facies and benthic habitats still persist due to some subtle
suitability models (e.g. Davies et al. 2008; Arantes et al. variations within the habitat itself that are scale- and
2009; Davies and Guinotte 2011; Buhl-Mortensen et al. resolution-dependent (Lurton and Lamarche 2015).
2012; Fabri et al. 2014, 2017; Robert et al. 2016; Bargain Despite some limitations, acoustic backscatter has been
et al. 2017; Lo Iacono et al., this volume). widely used for benthic habitat mapping, and several works
Slope, terrain roughness, BPI, and, to a lesser extent, have exploited seafloor acoustic backscatter for mapping
aspect and curvature, appear to be the best indices to mor- CWC habitat (e.g. Fosså et al. 2005; Roberts et al. 2009,
phologically describe suitable habitats for Mediterranean 2014), in particular in the Mediterranean Sea (Lo Iacono
CWCs (Cau et al. 2017; Fabri et al. 2017; Bargain et al. et al. 2008, this volume; Savini and Corselli 2010; Vertino
2017, 2018). For instance, Bargain et al. (2018) found that et al. 2010, this volume; Savini et al. 2014; Lastras et al.
these derivatives, each one calculated at a specific scale, are 2016). CWCs usually grow on hard substrates, which is gen-
the best indices to predict the most suitable surfaces for erally characterised by higher backscatter intensity com-
CWC presence in the Bari Canyon, Southern Adriatic Sea pared to softer bottom types (Lo Iacono et al. 2008; Savini
(Freiwald et al. 2009; Angeletti et al. 2014; Taviani et al. and Corselli 2010). Patches of CWCs also tend to display
2016). Using TASSE, we calculated the following morpho- typical backscatter patterns (e.g. cauliflower-like pattern:
metric attributes of this site (Fig. 16.3): relative difference to Fosså et al. 2005), which give information on coral coverage,
mean value (a relative position index, similar to BPI); local whether it is alive or dead (Roberts et al. 2009), morphology
standard deviation (a measure of roughness); eastness and and potential burial under sediment.
northness (similar to aspect); local mean; slope (computed as
per Horn 1981).
16.2.3 Sub-bottom Profiles
16.2.2 Backscatter Data Sub-bottom profiles are displays of the acoustic reflectivity
of the sediment layers below the seafloor, obtained through
Backscatter data is a measure of the acoustic reflectivity of the use of sub-bottom profilers or seismic sources. Sub-
the seafloor and is related to substrate composition and attri- bottom profiles have proven useful for the identification of
butes (Jackson and Briggs 1992). Backscatter is influenced CWC mounds and for the three-dimensional characterisation
also by incident angle, seafloor morphology (both at large of CWC bioconstructions (e.g. Masson et al. 2004; Fosså
and small scale, such as rugosity) and volume heterogeneity. et al. 2005; Roberts et al. 2005; Wheeler et al. 2005; Correa
Both MBES and side-scan sonar (SSS) systems can acquire et al. 2012; Somoza et al. 2014). In the Mediterranean Basin,
this type of data (Fig. 16.4a, b), although these systems have they have been used in the Tuscan Archipelago (Remia and
different conditions of acquisition and thus produce different Taviani 2005), Almería Margin (Lo Iacono et al. 2008),
results. This configuration results in a high sensitivity of SSS Santa Maria di Leuca (Taviani et al. 2005; Malinverno et al.
images to fine scale morphology (e.g. sand waves, cables, 2010; Savini and Corselli 2010) and Southern Adriatic Sea
wrecks, moorings and outcropping rocks: Lurton and (Taviani et al. 2016). A typical seismic signature of CWC
Lamarche 2015; Lamarche et al. 2016 and references colonies is acoustically transparent hyperbole on the seafloor
therein). (Savini and Corselli 2010; Taviani et al. 2016). While sub-
Backscatter data offer qualitative information on type of bottom profiles are a good tool to detect CWCs, especially
substrate (Hughes Clarke et al. 1996), a crucial element for on a seafloor characterised by coral mounds, the technique is
habitat mapping. High-intensity backscatter values are usu- less useful on canyon walls as the signal is noisy due to dif-
ally associated with hard substrates (cropping bedrock, over- fraction hyperboles caused by the high acclivity (e.g. Bari
consolidated sediments, hardgrounds, bio-constructions, Canyon: Trincardi et al. 2007).
Fig. 16.3 Terrain attributes

calculated for Bari Canyon
through TASSE toolset
(Lecours et al. 2015): (a)
bathymetric DEM, source for
the derivatives; (b) slope; (c)
local standard deviation of the
bathymetry (measure of
rugosity); (d) relative
difference to mean value
(rdmv; measure of relative
position); (e) northerness and
(f) easterness (measure of
slope orientation). (©
ISMAR-CNR Bologna)
16.3 Small Scale Data arm, or push corer, which provide information on macro- and
micro-benthic epifaunal and infaunal components, and is
The scale of acoustic data is often too large to accurately also propitious to assess textural and compositional
identify the seafloor type and morphology. The acquisition properties.
of small scale data (direct observations of the seafloor) then
becomes fundamental to validate habitat maps resulting from
acoustic data analyses (ground-truthing). Video footage or 16.3.1 Video Processing
photography of the seafloor are usually acquired through
cameras mounted on autonomous underwater vehicles Processing footage of photography acquired from AUV or
(AUVs), remotely operated vehicles (ROVs) or manned sub- ROV-mounted cameras into useful ground-truth data also
mersibles, and are usually mandatory to describe megaben- requires the analysis of the vehicle’s navigation, and its syn-
thic communities such as CWCs (e.g. Orejas et al. 2009; chronisation with the footage. There are several software
Vertino et al. 2010; Gori et al. 2013; Angeletti et al. 2014; packages specifically developed for handling underwater
Taviani et al. 2016, 2017). Other types of ground-truth georeferenced scientific video, such as ADELIE (a GIS-
include bottom sampling through grab, box-corer, robotic based software developed by IFREMER) and OFOP (Ocean
Fig. 16.4 Backscatter data

available for Bari Canyon
(a) – MBES backscatter and
SSS TOBI imagery – and
Montenegro slope (b, c) and
(d) visual interpretation of the
backscatter for the two sites;
automatic classification of
backscatter images through
RSOBIA validated with
seabed samples, for Bari
Canyon (e) and Montenegro
datasets (f). Obviously, the
resulting maps only
emphasises mobile sediment
as recorded by a very limited
number of grabs, disregarding
rocky substrate and bedrocks
at places overwhelming the
actual geology of the margins.
(© ISMAR-CNR Bologna)
Floor Observation Protocol: Huetten and Greinert 2008; While ROV video classifications provide “punctual”
Ludvigsen 2010). The synchronisation of video with naviga- information, a continuous spatial coverage can be obtained
tion allows georeferencing and capturing video-frames, cre- by operating a georeferenced collage of the video still
ating video summaries along the survey path. Subsequently, frames, effectively creating a photo-mosaic (Ludvigsen and
the analysis of still photographs can be represented through Soreide 2006). For this purpose, it is necessary that the
a classification of the AUV or ROV track according to sub- underwater vehicle navigates at a constant altitude from the
strate and benthic component. As for the Mediterranean Sea, seafloor. Several softwares are able to process images to pro-
this methodology has been applied to the Santa Maria di duce photo-mosaics, among them ADELIE OTUS (imple-
Leuca CWC province by Vertino et al. (2010). Here we pres- mented by IFREMER) and the freeware LAPMv2 (Marcon
ent a second case study focused on the Bari Canyon and 2016). Photo-mosaics allow one to map objects, such as spe-
Montenegro slope. We identify CWC habitats at fine scale cies or communities, manually (Wheeler et al. 2005; Roberts
using ROV video observation and classification of ROV et al. 2009) or automatically (Lim et al. 2017) over a continu-
tracklines according to CoCoNet classification scheme ous area. Largely applied to CWC habitat mapping in the
(Figs. 16.5 and 16.6) (Foglini et al. 2014; Angeletti et al. Atlantic Ocean (e.g. Porcupine Seabight, NE Atlantic:
2015b, 2016; Grande et al. 2015; Boero et al. 2016). Wheeler et al. 2005; Roberts et al. 2009; Lim et al. 2017), the
Fig. 16.5 (a) 3D view of

Bari Canyon bathymetry
(vertical exaggeration 10×)
and (b) backscatter data
draped on it (vertical
exaggeration 10×) with
localisation of the ROV track
(© ISMAR-CNR Bologna).
(c) Detail on the ROV track
mapped according to
CoCoNet classification
scheme for the substrate
(levels 1 and 2) and biological
component (levels 1, 2 and 3)
and georeferenced video still
frames along the track
showing (a) mixed substrate
with emerging rocks and
hardgrounds from muddy
sediments with mixed
aggregation dominated by big
fan-shaped sponges such as
Pachastrella monilifera and
stony corals (Madrepora
oculata: in background) and
(b) rocky substrate with
mixed aggregation of stony
corals (M. oculata in
foreground) and sponges (P.
monilifera in background)
(Photographs: a, b: ©
ISMAR-CNR Bologna)
only published example for Mediterranean CWCs is the surrogate (or marine landscape)) map has been produced by
photo-mosaic at Santa Maria di Leuca produced by Vertino integrating the geomorphological (Fig. 16.7) and substrate
et al. (2010). maps, obtained through manual interpretation of bathymetry
and backscatter data according to the classification scheme
of the European Project “Towards COast to COast NETworks
16.4 Cold-Water Coral Habitat Mapping of marine protected areas (from the shore to the high and
deep-sea) coupled with sea-based wind energy potential” –
The usual approach to map the distribution of CWC habitat CoCoNet (Fig. 16.4a–d: Foglini et al. 2014; Angeletti et al.
in the Mediterranean Sea is through an expert’s interpreta- 2015b, 2016; Grande et al. 2015) (Fig. 16.8). The benthic
tion of acoustic data, coupled with photographs of the sea- habitat map shows the distribution of CWC habitat in the
floor and bottom samples (Lo Iacono et al. 2008, 2012a, b; study area (Fig. 16.9), resulting from the addition of its bio-
Savini and Corselli 2010; Vertino et al. 2010). In our case logical component as derived from ROV images and bottom
study, the benthoscape (sensu Zajac et al. 2003; Brown et al. samples (Angeletti et al. 2014, 2015a, b; Taviani et al. 2016).
2012; Lacharité et al. 2017: the integration of geomorpho- The main issue of the above approaches is that they are
logical and substrate interpretation resulting in an abiotic subjective and time-consuming. A number of more automatic
Fig. 16.6 (a) 3D view of

Montenegro continental slope
bathymetry (vertical
exaggeration 10×) and (b)
backscatter data draped on it
(vertical exaggeration 10×)
with localisation of the ROV
track (© ISMAR-CNR
Bologna). (c) Detail on the
ROV track mapped according
to CoCoNet classification
scheme for the biological
component (levels 2 and 3)
and georeferenced video still
frames along the track
showing (a) Alcyonacean
assemblages typified by
monospecific forest of
Callogorgia verticillata
(Angeletti et al. 2014) and (b)
Antipatharian assemblages
characterised by Leiopathes
glaberrima and Antipathes
dichotoma (Angeletti et al.
2014)
approaches have been devised over the years. They can usu- be both automatically classified (e.g. Lecours et al. 2016
ally be categorised as either top-down or bottom-up (Brown with references therein).
et al. 2011). The input data for these methodologies can be bathyme-
try, its derivatives, or backscatter data, or often a combina-
tion of them. Top-down approaches using backscatter data
16.4.1 Top-Down Approach have been developed based both on signal (e.g. Angular
Range Analysis: Fonseca et al. 2009; Anderson et al. 2008)
Benthic habitat mapping top-down approaches are methods and on mosaic characteristics (e.g. Image texture analysis,
that classify input data with no supervision, based solely on TexAn: Blondel 1996; Principal Component Analysis:
the patterns and variation in the input data. Then, ground- McGonigle et al. 2009; Neural Network: Marsh and Brown
truth data may be used to identify the seascape, substrate 2009). Backscatter image analysis is the most common
(abiotic surrogates), species or communities characterising method for substrate and/or habitat classification because it
the classes (Fig. 16.1). Geomorphology (expressed by describes large-scale patterns of seafloor substrate and ben-
bathymetry and its derivatives) and seafloor backscatter can thic habitats better than backscatter signal analysis and can
Fig. 16.7 Manual
geomorphological
interpretation for Bari Canyon
(a) and Montenegro
continental margin (c) aided
by CHIRP sub-bottom
profiles (b). The shown
geomorphological
interpretation reflects the level
2 of CoCoNet classification
scheme (Foglini et al. 2014;
Angeletti et al. 2015b, 2016;
Grande et al. 2015). (©
ISMAR-CNR Bologna)
be performed with several GIS software (Lamarche et al. Once sampling is extended to consider all lithotypes and
2016 and references therein). Such analysis typically con- sediment types making up the considered margins, this
sists in segmenting the sonar image based on the local spec- OBIA exercise would be able to discriminate potentially
tral and spatial characteristics. The clusters are then grouped CWC-suitable substrates (Fig. 16.4e, f).
into homogeneous subsets through a process called classifi-
cation, based on user-specified combinations and can be
unsupervised or supervised. 16.4.2 Bottom-Up Approach
Using the freeware RSOBIA (Remote Sensing OBIA: Le
Bas 2016), we have segmented the TOBI image of the Bari Bottom-up, or supervised, approaches to habitat mapping
Canyon and the backscatter image of the Montenegro dataset consist in using the ground-truthing data (images and bottom
using an Object-Based Image Analysis (OBIA: Blaschke samples) to train the segmentation of the environmental data
2010) (Fig. 16.4e, f). In this process, the segmentation is (bathymetry and backscatter). In the following sections, two
based on the shape of the clusters and on their spatial correla- methodologies applied for CWC habitat mapping in the
tion (not only on their thematic similarity; Lamarche et al. Mediterranean Sea are discussed: (i) automatic classification
2016). The resulting OBIA segmentation was ground-truthed (supervised pixel-based image analysis of backscatter), and
using the sediment samples falling within each segment. (ii) CWC habitat suitability models.
Fig. 16.8 Benthoscape of the

sites of Bari Canyon (a) and
Montenegro slope (b)
obtained with the combination
of geomorphological and
backscatter manual
interpretation, following
scheme. (© ISMAR-CNR
Bologna)
16.4.2.1 Automatic Classification 6.4.2.2 Habitat Suitability Models

1
Supervised pixel-based image analysis is an automatic clas- The automatic classifications depicted so far allows for a
sification method applied to characterise CWC habitats and description of the physical and biological components of
their distribution. Maximum Likehood classification, Iso CWC habitat as well as mapping their spatial distribution
Cluster and Textural analysis (using Grey Level and variations within a surveyed area. However, such statisti-
Co-occurrence Matrices) are algorithms developed to carry cal analyses can also be used to predict the areas that are
out supervised pixel-based image classifications and have prone to host this habitat. This procedure is called Habitat
been applied in Mediterranean CWC sites (Savini et al. 2014; Suitability Modelling (HSM) and is achieved through differ-
Lo Iacono et al., this volume). ent methods, such as Ecological-Niche Factor Analysis
Maximum Likehood and Iso Cluster algorithms were (ENFA: developed by Hirzel et al. 2002), Maximum Entropy
used to segment bathymetry and its derivatives to identify the modelling (Davies and Guinotte 2011; Yesson et al. 2012;
seafloor morphologies that are likely to support Anderson et al. 2016) and Generalised Linear Models
CWCs. Textural analysis was used to quantify and identify (Woodby et al. 2009; Rengstorf et al. 2014). Most of the
backscatter image textures and patterns. This analysis was CWC habitat suitability models developed to date were in
instructed using training zones chosen by experts (seafloor the Atlantic Ocean (e.g. Leverette and Metaxas 2005; Davies
areas where substrate type and biological assemblages are et al. 2008; Dolan et al. 2008; Guinan et al. 2009a, b; Robert
known thanks to ground-truth data), in order to classify the et al. 2014, 2016), or at a global scale (Bryan and Metaxas
nature of substrate and benthic habitat (Blondel 1996). 2007; Tittensor et al. 2009; Yesson et al. 2012). Recent HSM
Fig. 16.9 Map of the benthic

habitat for Bari Canyon (a)
and Montenegro continental
margin (b) built following
scheme. (© ISMAR-CNR
Bologna)
applications of CWCs in the Mediterranean Sea (Cassidaigne to each variable according to its contribution to CWC prefer-
Canyon: Fabri et al. 2017; Santa Maria di Leuca and Bari ence of a specific area. The validation is carried out using
Canyon: Foglini et al. 2016b, 2017; Bargain et al. 2017, CWC presence-only data and the result is a probability map
2018) identified MaxEnt as the best method to predict CWC highlighting the potential sites for CWC growth.
habitat distribution in terms of probability of occurrence. While CWC habitat mapping produces a snapshot of the
Such an approach makes use of geomorphometric deriva- distribution of the habitat at the moment of the survey, HSM
tives and oceanographic variables (i.e. temperature, salinity, represents a step forward by mapping the potential for future
currents velocity) as input dataset and trains the model with distribution. They are performed on well-known CWC sites
presence-only data (occurrences of CWC coming from bot- in order to choose and train the best model able to automati-
tom samples and ROV images). The model assigns a weight cally find other areas suitable for CWC settling.
16.5 C
old-Water Coral Habitat Mapping The best acoustic resolution can be achieved either by
Techniques Caveats and Perspectives towing instruments near the bottom (like for SSS) or, more
commonly, by instrumenting ROVs or AUVs (e.g. Grasmueck
We have presented the different types of data (Table 16.1) et al. 2006, 2007; Huvenne et al. 2011, 2016b; Wynn et al.
and techniques used for CWC habitat mapping in the 2014). This kind of vehicles can follow the topography and
Mediterranean Sea. Top-down vs bottom-up approaches to mounting the MBES vertically on a ROV would allow for
CWC habitat mapping depends upon type, amount and high-resolution surveys of subvertical walls, cliffs or head-
quality of data. The first one is generally used when the wall scarps generating also a 3D reconstruction. Some exam-
available data cover large areas with a coarse spatial reso- ples are presented in Huvenne et al. (2011, 2016b) and
lution and include scarce or no ground-truthing data. The Robert et al. (2014) on the CWC-dominated walls of the
second approach is applied when an extensive ground- Whittard Canyon. However, this technique has not yet been
truthing dataset is available, allowing one to train models applied to Mediterranean CWC sites.
or interpret and validate the results. Both approaches rely Bottom samples are fundamental to determine the nature
upon automatic classification algorithms that have been of substrate (hard, soft or firm) and sediment texture and to
rarely implemented for CWC habitat in the Mediterranean validate backscatter interpretation (manual or automatic) for
Sea to date. This is probably because geophysical data are top-down approaches or train bottom-up classification
currently only available at a spatial resolution that is too algorithms.
coarse to distinguish features and patterns related to CWC Visual inspection is used for first hand qualitative sub-
colonies. strate assessment and for biological identification. High defi-
Table 16.1 Table showing the data required for benthic habitat mapping, the information and advantages that we get using them and their limits
Data Devices for acquisition Info and advantages Limits
Bathymetry MBES (and single Water depth (m) Indirect method (remote sensing)
beam echosounders) Seafloor morphology Spatial resolution not always adequate
Manual geomorphological interpretation to measure ecological processes
Geomorphometric analysis to support interpretation and
extract geomorphological features
Large scale to fine scale data
High spatial resolution
Acoustic MBES and SSS Information on seabed substrate (hard/mobile, grain Indirect method
backscatter size)
Enhance some geomorphological features Noisy
Qualitative and quantitative (only MBES backscatter) Influenced by incident angle and
analyses morphology/rugosity
Manual and automatic classification Shadows (SSS backscatter)
Large scale to fine scale data Spatial resolution not always adequate
to measure ecological processes
High spatial resolution Signal penetrates the sediments
Possible discrepancy between acoustic
response and seafloor substrate
CHIRP profiles Sub-bottom profiler High resolution stratigraphy (penetration of few metres) Low penetration
(SBP) Support morphological and backscatter interpretation 2D information
Detection of morphologies related to specific habitats
(e.g. coral mounds)
Seafloor Grab, box corer, corer, Ground-truth data for acoustic data analysis Punctual database
samples dredge, hauls Information on seafloor geology (lithology, grain size) Discrepancy in scale between
Information on mega- and macro-epifauna and infauna geophysical data and seafloor samples
Information on palaeobiology
ROV video and Camera Ground-truth data for acoustic data analysis Very fine scale → discrepancy in scale
images between geophysical data and seafloor
images
HD images of seascape, seafloor and habitats ROV exploration → linear data
Detailed information on habitats: identification of
species, extension, density, health of the organisms, etc.
Photo-mosaic → mapping at fine scale → bridge
between large and fine scale analyses
nition images, currently up to ultra-high definition (4k), processed the data, and finally performs an automatic fine-
extracted from cameras mounted on ROVs, permit one to scale identification of species or communities, to be com-
identify not only mega-benthic, but even macro-benthic pared with a library of spectral fingerprints (Pettersen et al.
organisms (>20 mm), to the lowest possible taxonomic rank 2014; Johnsen et al. 2016; Foglini et al. 2018). The construc-
(species). Further data extracted from ROV images are fun- tion of the library is a critical prerequisite that will require an
damental to contribute to satisfy the requisites of programs important and coordinated effort in order to fit all possible
such as MSFD (EU Marine Strategy Framework Directive) situations to be found in the ocean.
aimed at monitoring Good Environmental Status (GES) of Another recent development in habitat mapping is the use
benthic habitats, with the lowest possible impact on the sea- of oceanographic data. Indeed, oceanographic variables are
floor. Despite its diffused application for CWC habitat map- important in species and habitat distribution, so that habitat
ping in Europe and elsewhere, just one study exploited inventories and classification schemes (e.g. CMECS:
photo-mosaic of ROV images within the Mediterranean Madden et al. 2009; EUNIS: Garlparsoro et al. 2012) have
region (Vertino et al. 2010), while the application of georef- considered oceanographic variables for habitat characterisa-
erenced photo-mosaics to Mediterranean CWCs is highly tion. Nevertheless, oceanography is only seldom considered
desirable. Nevertheless, biological samples are needed in in CWC habitat maps and is by now contemplated to be
most cases to properly assess taxonomy. In fact, a large num- included in Habitat Suitability Models calculations as mod-
ber of taxa cannot be identified from images at species-level, els of variables (not as long-term measurements), with a spa-
such as some cnidarians or sponges, which were described as tial resolution much coarser than those of acoustic or
morpho-species or morphological categories in some works ground-truth data (Vincent et al. 2004; Kostylev and Hannah
(e.g. Bell and Barnes 2001). 2007; Degraer et al. 2008; Verfaillie et al. 2009; Brown et al.
Seafloor backscatter images are seldom analysed for 2011). Regarding the Mediterranean basin, oceanographic
CWC habitat mapping and HSM. Any interpretation of the variables have been included in models of CWC habitat suit-
seafloor substrate based solely on acoustic reflectivity pres- ability in the Bari Canyon and Cassidaigne Canyon (Bargain
ents some caveats which can be relevant for CWCs and habi- et al. 2018).
tat mapping. High reflectivity (high backscatter intensity) is Besides the new sources of data introduced previously,
usually interpreted as an indication of hard bottom (rock or developments are also expected in the classification algo-
gravel), when it could be in reality draped by soft sediments. rithms themselves. Recently introduced methods with high
In such a case, the retro-diffused signal responded predomi- potential are multi-model ensembles, which integrate differ-
nantly to an underlying hard substrate more than to the ent automatic methods, both unsupervised and supervised,
easily-penetrable thin muddy drape. Backscatter data are without omitting any fundamental aspect for habitat map-
also influenced by the morphology showing higher intensity ping (Diesing et al. 2014). Thus far, the expert’s interpreta-
in correspondence to steep slopes, such as scarps and canyon tion is the most adopted approach serving CWC habitat
flanks that can be covered by a muddy layer. These examples mapping in the Mediterranean basin since fundamental to
illustrate the inherent ambiguity of backscatter data, and thus assign a meaning to the classes in which the datasets can be
the fundamental obligation to validate any interpretation. In segmented. It appears, therefore, advisable to find the opti-
addition, backscatter data from MBES are not calibrated to mal combination of methods for mapping and modelling
date, although efforts have recently been made in this direc- Mediterranean CWCs.
tion (Lurton and Lamarche 2015). Calibrated MBES in the
future would help in overcoming these possible discrepan-
cies between backscatter signal interpretation and seafloor 16.6 Conclusions
composition. Progress in multibeam technology, such as
multi-frequency systems, is also expected to bring about fur- It is urgent to establish measures for the sustainable manage-
ther accuracy in habitat mapping (Hughes Clarke 2015; ment of such emblematic ecosystems of the deep which are
Brown et al. 2017). increasingly threatened by climatic and anthropogenic
Another promising technology to improve and accelerate stressors. The integration of habitat mapping methodologies
the recognition of salient biological traits in a given deep- and habitat suitability models is instrumental to deal with
water habitat (such as CWCs) would be the use of hyper- these societal problems. Habitat mapping evolves continu-
spectral cameras. For example, The Underwater ously, following the implementation of existing techniques
Hyperspectral Imager (UHI) developed by Ecotone is a ROV as well as technological ameliorations and advances in
equipped with hyperspectral cameras and a suite of data pro- marine sciences. Hence, future innovative approaches will
cessing algorithms. This system records upwelling radiance strengthen its potential and efficacy in the coming years. The
or reflectance in the entire visible band (390–700 nm) with mapping of Mediterranean CWC ecosystems is still in its
up to 1 nm resolution, and radiometrically and geometrically infancy, but is steadily gaining momentum due to the increas-
ing scientific outcomes. Habitat mapping is a valuable tool to and deep sea), coupled with sea-based wind energy potential. SCI
RES Inform Technol Ric Sci Tecnol dell’Inform 6:1–95. https://doi.
improve the characterisation and evaluation of the status of org/10.2423/i22394303v6Sp1
Mediterranean CWCs by fostering a better accuracy of CWC Bonaldo D, Benetazzo A, Bergamasco A, et al (2016) Interactions
occurrences in terms of geo-biological and oceanographic among Adriatic continental margin morphology, deep circulation
aspects and predicting potentially-suitable CWC settings. and bedform patterns. Mar Geol 375:82–98
Brown CJ, Smith SJ, Lawton P, et al (2011) Benthic habitat mapping:
a review of progress towards improved understanding of the spa-
Acknowledgements We are indebted to editor Covadonga Orejas, tial ecology of the seafloor using acoustic techniques. Estuar Coast
Stefan Ekehaug and an anonymous reviewer for their critical comments Shelf S 92:502–520
that significantly helped to improve the present chapter. English lan- Brown CJ, Sameoto JA, Smith SJ (2012) Multiple methods, maps, and
guage has been kindly revised and improved by William McKiver. This management applications: purpose made seafloor maps in support
paper is ISMAR-Bologna scientific contribution n. 1930 and is part of of ocean management. J Sea Res 72:1–13
EU F.P. VII Projects CoCoNet, (contract no. 287844), and EVER-EST Brown CJ, Beaudoin J, Brissette M, et al (2017) Setting the stage for
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(grant agreement No. 11.0661/2017/750680/SUB/EN V.C2), and the CJ, Lacharité M, et al (eds) Program and abstracts GeoHab confer-
Flag Project Ritmare (Ricerca Italiana per il Mare) projects. ence. Nova Scotia Geological Survey of Canada, Dartmouth, Open
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Drop Chapter
Working with Visual Methods, 17
Comparison Among the French Deep-
Sea Canyons
Maïa Fourt, Adrien Goujard, and Pierre Chevaldonné
Abstract the western coast of Corsica (CorSeaCan) with the aim of

The MedSeaCan and CorSeaCan cruises (November exploring the benthic ecosystems associated to deep-sea can-
2008 to August 2010) took place along the French conti- yons. The study area spanned from 3°35′ to 9°35′E and from
nental shelf, from the Spanish border to Monaco 41°25′ to 43°70′N (Fig. 17.1). The canyons, and nearby
(MedSeaCan) and the western coast of Corsica rocky banks (geological features rising a few meters from the
(CorSeaCan). They provided a reference state of the eco- surrounding flat continental shelf, here generally near the
system in the general context of deep-sea canyons, head of canyons) were explored from 34 to 802 m depth,
through direct observations with a remotely operated with a main focus between 100 and 600 m. A total of 34
vehicle and a human occupied vehicle. Both devices col- canyons and 9 rocky banks were investigated through 475 km
lected photographic, video and biological samples, and all of prospection by 264 dives with a “Super Achille” type
have been integrated in the specifically designed remotely operated vehicle (ROV) and 23 with the “Rémora
ZOOlogical Data Exploitation system working platform 2000” human occupied vehicle (HOV); mean distance
(Goujard and Fourt. 31 October 2014). These cruises explored in canyons was 12.5 km (min. 1 km, max. 27.5 km).
were the very first attempt to systematically explore Surveys were all conducted on board the Research Vessel
French Mediterranean deep-sea canyons. The same data ‘Minibex’ which was geolocalised by a submetrical GPS and
acquisition techniques were used throughout the cruises able to localise the ROV by means of a transponder, provid-
and the same scientific team treated the data. Extensive ing tracks at a cm level precision.
remotely operated vehicle exploration appears to be an As a first step, bathymetrical exploration of the canyons
appropriate method for comparing canyons and better was conducted to identify the steepest flanks. Prospection by
apprehend cold-water coral distribution. Moreover, this ROV took place going up the steepest flanks and canyon
method gives the possibility to initiate a monitoring pro- heads perpendicularly to the isobaths, from 600 m depth to
gramme of the deep-sea benthos. the shelf-break. The ROV video transects covered a ca. 3 m
wide section, the ROV speed was non-constant (around
Keywords 850 m h−1) as it was decided depending on the occurring
Submarine canyons · Cold-water corals · Mediterranean · fauna. All transects were filmed at least by a low definition
Visual method survey · ZOODEX Platform Pan and Tilt camera cumulating 550 h of video records. A
total of 21,900 pictures were taken, including species, habi-
tats, anthropogenic impacts and substrate. Further, HD
The MedSeaCan and CorSeaCan cruises took place from images were taken when a poorly known species or assem-
November 2008 to August 2010 along the French continental blage was detected, when a species showed a specific behav-
shelf, from the Spanish border to Monaco (MedSeaCan) and ior and also when areas with high biodiversity were
encountered (Fourt et al. 2014). Two laser beams 6 cm apart,
M. Fourt (*) · P. Chevaldonné provided a scale enabling some sample measurements. Beside
IMBE, CNRS, Aix Marseille Université, Avignon Université, the video and photo material, 320 samples were collected
IRD, Station Marine d’Endoume, Marseille, France
(biological samples, substrate, water) by ROV or HOV.
From the video/photo material and from the samples the
A. Goujard
following information was extracted and quantified: occur-
GIS Posidonie, Marseille Cedex 09, France
rence of taxa, litter, trawling marks and changes in facies
COMEX S.A., Marseille Cedex 09, France

https://doi.org/10.1007/978-3-319-91608-8_17
192 M. Fourt et al.
Fig. 17.1 Location of the 43 sites (canyons and rocky banks) explored Canyon, 21: Magaud Bank, 22: Stoechades Canyon, 23: Nioulargue
during the MedSeaCan and CorSeaCan cruises. 1: Lacaze-Duthiers Bank, 24: Pampelonne Canyon, 25: Saint-Tropez Canyon, 26: Dramont
Rocks, 2: Lacaze-Duthiers Canyon, 3: Pruvot Canyon, 4: Sète Rocks, 5: Canyon, 27: Méjean Seamount, 28: Cannes Canyon, 29: Juan Canyon,
Bourcart Canyon, 6: Marti Canyon, 7: Ichtys Bank, 8: Sète Canyon, 9: 30: Nice Canyon, 31: North Centuri Canyon, 32: South Centuri Canyon,
Montpellier Canyon, 10: Petit Rhône Canyon, 11: Grand Rhône 33: Saint-Florent Canyon, 34: Ile Rousse Canyon, 35: Calvi Canyon,
Canyon, 12: Couronne Canyon, 13: Planier Canyon, 14: Cassidaigne 36: Galeria Canyon, 37: Porto Canyon, 38: Cargèse Canyon, 39: Sagone
Canyon, 15: Esquine Bank, 16: Blauquières Bank, 17: No-Name Canyon, 40: Ajaccio Canyon, 41: Valinco Canyon, 42: Les Moines
Canyon, 18: Sicié Canyon, 19: Toulon Canyon, 20: Porquerolles Canyon, 43: Asinara Bank
and substrates; each of these observations constituted an neous treatment of the data. Georeferenced and time-coded
“event” along the prospection tracks. The data obtained, events of each dive were described by variables related to:
was organised and interconnected in the ZOODEX the identification of species, the number of individuals, the
(ZOOlogical Data EXploitation system) working platform nature of the substrate, the presence of given facies of
(Goujard and Fourt 2014), which provided a friendly envi- CWCs, qualitative description of the bioturbation (catego-
ronment in which to plot observations and extract informa- ries used: absent, low, medium, high) and the sessile and
tion (see Fig. 17.2). ZOODEX was specifically designed mobile biodiversity (categories: low, medium, high), the
for: (1) systematic and homogeneous processing of under- presence of waste, plankton occurrence, trawl marks, the
water images along a dive track, (2) storage and linking of collection of a biological, substrate or water sample, as well
data (e.g. photographs, video footage, and samples which as any other potential comment or observation from the
offer information on the substrate type, habitat and species observers. Consequently, each event is contextualised and
identification), (3) easy access and retrieval of the informa- linked to a dive, a video sequence and to one or several pho-
tion and, (4) spatial and temporal comparisons (e.g. vari- tographs (when available) as shown in Fig. 17.2. Species
ability of the bathymetrical distribution of a species within identification was conducted using the photographic and
the sites explored). At the core of the system, a Microsoft® video material, with the support of a group of 25 specialists
Access 2010 database is coupled with a GIS (Geographic in taxonomy; moreover the identification was occasionally
Information System). The ZOODEX was used for the post performed using biological samples when available. The
processing of the photographs and video footages. The ZOODEX allows to display the information, images and
visual material (photographs and video) was analysed by maps, using different filters such as species names, depth
the same scientific team which highly guarantees a homoge- range, sites, habitats, and substrate types as possible entries.
17 Working with Visual Methods in French Deep-Sea Canyons 193
The surveys presented in this chapter covered only a few spotted in places where the species was previously unknown
CWC hotspots. These included live Lophelia pertusa such as Bourcart, Sicié and Nice canyons. Although Corsican
occurring only in the Lacaze-Duthiers canyon between 250 canyons did not show any of these two CWC species, Les
and 535 m depth on rocky cliffs, where it formed dense Moines canyon revealed marl walls unexpectedly covered by
patches with Madrepora oculata, but also on silted slopes. In large populations of the solitary deep-sea coral Desmophyllum
Cassidaigne canyon, large areas were covered by M. oculata dianthus between 453 and 617 m (Fig. 17.3). In continental
in a particularly shallow context from 196 to 250 m, along canyons, D. dianthus had only been documented as isolated
with circalittoral species such as the gorgonian Paramuricea specimens among the other CWCs, however recently a large
clavata. Some isolated colonies of M. oculata were also facies of D. dianthus has been discovered in La Fonera can-
Fig. 17.2 Schematic view of the methodology used for the MedSeaCan such as (top to bottom): bathymetrical distribution of a species at sites
and CorSeaCan research cruises. Step 1 consists in the data acquisition where it occurs, interactive track map with linked events, substrates and
including the geolocalised video and photographs; Step 2 includes the photos, table of time-coded observations for a dive with associated
data treatment with the ZOODEX platform; Step 3 displays outputs information
Fig. 17.3 Desmophyllum dianthus covering a marl wall at Les Moines deep-sea canyon, western Corsica, 476 m. The carapace of the squat lobster
Munida sp. measures about 3 cm. (Photo COMEX/Agence française pour la biodiversité - campagne CorSeaCan)
194 M. Fourt et al.
yon (Catalan margin) (see Aymà et al., this volume; Lastras evaluation of the state of conservation of the communities.
et al., this volume). In Les Moines canyon, associated fauna Further, this method also offers the possibility to return to
consisted of deep-sea oysters Neopycnodonte zibrowii (occa- specific locations and specific individuals (e.g. CWC colo-
sionally observed alive), carnivorous sponges Cladorhiza cf. nies) to evaluate potential changes over time. The 3D recon-
abyssicola and Lycopodina hypogea, as well as teleost fish struction of targeted populations may also be appropriate
such as Benthocometes robustus (see images in Fourt et al. for the survey of population dynamics in selected specific
2017). areas.
Using an ROV combining a primary low definition con-
tinuous video recording together with on-demand HD video/ Acknowledgements We are grateful to the “Agence des Aires Marines
photo acquisition, allows covering and documenting Protégées” (now “Agence française pour la biodiversité”) for support-
ing the cruises and their data treatment. We also thank the Comex SA
extended geographic areas in a fairly short time, while team and the MedSeaCan and CorSeaCan scientific teams.
obtaining high quality images of locations and/or specimens.
In the specific case of CWCs, this system offers the possibil-
ity to precisely document their occurrence, information that
is essential for conservation and management plans. References
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past ROV track based only on geographical positioning de suivi temporel 2D en zone profonde & Apport de l’imagerie 3D
appeared too complex. However, it was possible to follow a à la description et au suivi temporel des communautés de grottes
path plotted with remarkable reference points originating sous-marines et des roches profondes. Partenariat «Grottes 3D &
from the initial ROV track. Revisiting the same sites demon- MedSeaCan 3D». IMBE-CNRS/GIS Posidonie/Comex SA/Parc
National des Calanques/Agence des Aires Marines Protégées No.
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classes (Fourt et al. 2016).
The data collected during the cruises and processed in
the ZOODEX, supply information on spatial and bathymet- Cross References
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of the main megabenthic assemblages as well as on their Aymà A, Aguzzi J, Canals M, et al (this volume) Occurrence of living
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Sea
Review of the Circulation
and Characteristics of Intermediate 18
Water Masses of the Mediterranean:
Implications for Cold-Water Coral
Habitats
Daniel R. Hayes, Katrin Schroeder, Pierre-Marie Poulain,

Pierre Testor, Laurent Mortier, Anthony Bosse,
and Xavier du Madron

This chapter describes the main features of the circulation
and properties of the intermediate water masses of the In this paper, the current understanding of the flow and char-
Mediterranean. Interaction with other water masses is acteristics of intermediate Mediterranean Sea water masses
also briefly summarised. Both observational and numeri- is described. The motivation to include oceanographic stud-
cal studies described in the literature are used, as well as ies in this book is that ocean flows and water properties
some more recent, unpublished data sets. It is shown that establish the basic environmental conditions to which sessile
the main water mass important to cold-water coral habi- organisms are subjected. If conditions are favorable, in terms
tats is the Levantine Intermediate Water which forms in of temperature, salinity, dissolved oxygen, and organic mat-
the Levantine Sea, Eastern Mediterranean and spreads ter, all of which are maintained adequately by the currents,
throughout the entire Mediterranean before leaving via then cold-water corals (CWC) can thrive. Johnston and
the Gibraltar Strait. This pathway is described as well as Larson (this volume) explain how the functionality and con-
the expected temperature and salinity along that pathway. nectivity of CWC are driven both by physical and biological
Current speed regimes are estimated from the few studies processes, merged through biophysical modeling. Before
that exist. robust results can be derived from biophysical modeling, the
performance of the flow modules must be evaluated against
Keywords the existing observational and numerical bodies of work pre-
Mediterranean sea · Hydrography · Circulation · sented in this chapter.
Intermediate water · Deep water · Cold-water corals In the Mediterranean, as will be described below, evapo-
ration exceeds precipitation when averaged over the basin,
and the “reverse estuarine” circulation that results implies a
D. R. Hayes (*)
net inflow into the basin (through the Gibraltar Straits). This
Oceanography Center, University of Cyprus, Nicosia, Cyprus
e-mail: [email protected] low input of river runoff, combined with the vertical stability
of the thermohaline circulation, make the waters relatively
K. Schroeder
Istituto di Scienze Marine, Venezia, Italy poor in nutrients. Thus, any process that injects nutrients into
the ocean, such as deep or intermediate water formation,
P.-M. Poulain
Istituto Nazionale di Oceanografia e di Geofisica Sperimentale, dense water cascades, or downwelling events around eddies,
Trieste, Italy will control the vitality of the ecosystem along the path of the
P. Testor · L. Mortier currents carrying the signal of these processes. Therefore,
CNRS-Sorbonne Universités (UPMC Univ. Pierre et Marie Curie, the conditions described here provide context for the regions
Paris 06), Paris, France where CWC have been discovered. Taviani et al. (2017) and
A. Bosse Taviani et al. (2011) (and references therein) identified five
Geophysical Institute, University of Bergen and Bjerknes Center discrete provinces: the Southwestern Adriatic, the Northern
for Climate Research, Bergen, Norway
Ionian, the Sicily Channel, the Alborán Sea, and the Catalan-
X. du Madron Provençal-Ligurian canyons, and more recently the Nora
CEFREM, Perpignan, France

https://doi.org/10.1007/978-3-319-91608-8_18
196 D. R. Hayes et al.
canyon, offshore Sardinia. Live CWCs have also been found preponderance of information for the eastern Mediterranean
in other places such as scleractinian corals on Eratosthenes characteristics and flows. One of the reasons for this is the
Seamount (Galil and Zibrowius 1998; Mitchell et al. 2013), present lack of a systematic review of the LIW in the eastern
and on the Anaximenes ridge summit south of Turkey, black basin. Besides being of interest in its own right, such a review
Antipathes coral and occasional Desmophyllum corals were may provide insight to the apparent low rates of recovery of
observed (Raineault et al. 2013). Epibenthic communities on CWC habitats in the eastern basin compared to the western
the Anaxagoras seamount hosted cold-water octocorals basin after pan-Mediterranean depletion in the late Pleistocene
(CWCs) and scleractinian corals (Shank et al. 2011). There (Taviani et al. 2011, Taviani, this volume; Vertino et al., this
is new evidence of CWC communities in the Cassidaigne volume). It may help answer the question: “how do today’s
Canyon on the Provençal east of the Gulf of Lion between conditions compare to those of the early Holocene?”
Marseille and Toulon at depths of the intermediate water
(around 500 m) (Fabri et al. 2017). Particular emphasis will
be given to flow and water properties at the depths at which 18.2 Approach
CWC are known to thrive: 350–600 m (Taviani et al. 2011),
which corresponds to intermediate water masses. A map of This study focuses on the current understanding of the pres-
the regions where these ocean depths are found is shown in ent-day characteristics and circulation, water mass pathways
Fig. 18.1, along with the confirmed CWC discoveries above. and currents of the Mediterranean below the surface layer
Deep water masses will also be briefly described since and above the deep layer. Because of the large spatial and
they are directly linked to the intermediate water through temporal gaps in the observational data sets available, in par-
mixing. Near-surface layers are also briefly described since ticular for subsurface layers, this understanding is based on a
they influence the production and volume flux of the variety of sources. Firstly, historical observations, going
intermediate water masses. Also, in certain places, during back to the early to mid twentieth century provide a low res-
dense water formation events, the seafloor may have direct olution set of static views. Naturally, changes have occurred
contact with the surface layer, or indirectly through the over this time period, many of them probably not known to
lateral spreading or downward cascading of these newly- us because of the sparseness of the observations. In order to
formed waters. piece together a coherent structure, however, we must glean
After a description of the approach taken, the paper pres- the essential information from these data sets and make con-
ents processes related to the spotty, intermittent intermediate clusions about what is a reasonable mean state.
water mass formation and transformation. The identifying Newer, unpublished, data sets certainly exist, and a few
characteristics, pathways and flow speeds of the Levantine examples related to the authors’ work are presented below.
Intermediate Water (LIW) are discussed in the final part of the In general, these include CTD cruises, eXpendable
paper, in subsections for the eastern and western BathyThermographs (XBTs), profiling floats, gliders and a
Mediterranean, respectively. The reader will recognise the few fixed point stations. These platforms measure
Fig. 18.1 Mediterranean basin and depths at which cold-water corals may be found (dark grey). Stars indicate known locations of living cold-
water corals (see references in text). Green triangle is position of CSNet mooring (data in Fig. 18.10). (Source of bathymetry is EMODnet 2017)
18 Intermediate Water Masses of the Mediterranean and Cold-Water Coral Habitats 197
temperature, conductivity (except XBT), and pressure. In In this chapter, the current steady-state view emerging
many cases, dissolved oxygen is also measured, but from the literature is described, while acknowledging that
chlorophyll, nutrient, and inorganic carbon data are sparse. this is a gross simplification, constantly violated by the rapid
Very few platforms measure properties below 1000 m, and transients and long-term changes mentioned above. Despite
even fewer measure currents directly (at any depth), making these violations, the steady-state view is useful as a starting
characterisation of deep flows extremely difficult. For this point upon which to base a detailed discussion of cross-basin
reason, currents are usually estimated using the assumption interactions and to understand the relevant processes and
of geostrophic balance, which is wrought with pitfalls in the likely ways that said transients spread around the basin.
Mediterranean, in particular because of an unknown A summary of what is known about the water masses and
reference at the typical maximum observation depth. It formation processes is provided in the next section, after
should be noted that satellite altimetry (dynamic height and which the spreading and pathways of those water masses are
Sea Level Anomaly: SLA) can also aid in calculating ocean discussed.
currents in a depth-averaged (barotropic) sense, but the
intermediate flow may not coincide because of stratification
(baroclinic flows). In some regions, these complementary 18.3 Water Masses
observation platforms have been organised into observatories
which operate for extended periods, often providing near By far, the dominant water mass at depths of 150–400 m and
real-time information, and associated prediction and 350–600 m in the eastern and western Mediterranean
assimilation products. For example, the MOOSE in France (respectively) is the Levantine Intermediate Water (LIW). In
captured processes related to deep and intermediate water fact, it is the most voluminous water mass produced in the
formation, as in Houpert et al. (2016) and Bosse et al. (2016). Mediterranean (Skliris 2014; Lascaratos 1993). The LIW is
Where relevant, these have been identified as a potential found throughout the Mediterranean, not just the Levantine
source of information that could be analysed further to region in which it forms (Fig. 18.2). Other intermediate
enhance the present, primarily retrospective, study. water masses include the Western Intermediate Water (WIW)
One exception to the lack of observable changes is the formed by wintertime cooling of Atlantic Water (AW) in the
striking example of the shift in the formation of the Eastern Western Mediterranean and the Cretan Intermediate Water
Mediterranean Deep Water (EMDW), in the 1990s, and later (CIW) formed in winter time and mostly trapped in the
the Western Mediterranean Deep Water (WMDW), both of Aegean Sea. The CIW was first identified by Schlitzer et al.
which indirectly affect the overlying intermediate water (1991) and defined to be Aegean water that spreads out into
properties (see below). Another example of observed change the Levantine and Ionian at 500–1200 m, i.e., below
is the ongoing change in salinity of the Mediterranean (see LIW. These two intermediate waters are produced in much
Skliris, this volume). Despite these exceptions, most lower quantities and their pathways are not easily identified
observational data sets are inadequate to describe the spatial (Millot and Taupier-Letage 2005a). However, it has been
or temporal variations, especially in the intermediate layer shown by Millot (2013) that the Aegean/Cretan waters con-
which is expected (and sometimes observed) to be tribute significantly to what some call the LIW in the western
tremendously complex. Surface layer variability is likely basin, so the name Eastern Intermediate Water (EIW) was
even more complex, but remote sensing and surface drifting suggested.
platforms have provided a realistic glimpse (Menna et al.
2012; Poulain et al. 2012; Rio et al. 2014).
For these reasons, a second source of information is often 18.3.1 The Functioning of the Mediterranean
used: numerical models and their associated re-analysis data Sea
sets. While theoretical considerations and hydrodynamic
simulations of varying complexity help in understanding the Future climatic changes will strongly affect the so-called
important processes of intermediate water mass climatic hot-spots regions, and the Mediterranean region is
transformation and spreading, and can even provide accurate one of them. Its climate is mainly influenced by the pres-
estimates of water mass production rates and exchanges ence of the sea, a “miniature ocean” in which typical
through straits, they are notoriously bad at prediction or oceanographic processes of the global ocean occur with a
reconstruction of the true ocean state. Nevertheless, through much shorter turnover timescale (one order of magnitude
the merging of observational data sets with dynamic less that the global ocean’s one). The expected rapid
formalisms (data assimilation), realistic ocean state estimates response of this water body to the variable atmospheric
can be made and are examined here in addition to published forcings is documented by a considerable amount of stud-
and ongoing observational studies and a thorough review of ies about changes in Mediterranean water mass properties
the Mediterranean structure and dynamics from a 20-year and rates of Dense Water Formation (DWF) (e.g., Bethoux
reanalysis from Pinardi et al. (2015). and Gentili 1999; Rixen et al. 2005; Schroeder et al. 2006,
2008).
Fig. 18.2 Vertical section

along trans-Mediterranean
section (a) of (b) potential
temperature, (c) dissolved
oxygen, (d) salinity, and (e)
potential density anomaly.
Levantine Intermediate Water
layer growing in thickness
and deepening as it spreads
from East to West (right to
left) indicated by potential
density anomaly between
28.85 and 29.1 kg m−3.
(Source of data: Tanhua et al.
2013)
There are three main circulation cells: a pan-Mediterra- exits the Mediterranean in the bottom layer at Gibraltar. An
nean one, an Eastern Mediterranean one, and a Western excellent summary of the above with references is provided
Mediterranean one (the latter two separated by the Sicily by Malanotte-Rizzoli et al. (2014) as well as Tsimplis et al.
Channel with a sill depth of about 500 m). The uppermost (2006). A schematic is shown in Fig. 18.3. A summary of
one is open and brings AW: 15 °C, 36.2) in through the Strait Mediterranean deep and intermediate water formation is pro-
of Gibraltar (sill depth of about 300 m) to make up for the net vided next.
evaporative losses of the basin. Other masses not formed in
the basin include the Black Sea Water and river input. These
are restricted to the surface and are not directly relevant to 18.3.2 Deep Water Formation
CWC habitats. They do, however, have an effect on the for-
mation of the deeper water masses. Intermediate water with The formation of deep water is briefly summarised here in
properties of approximately (13.5 °C, 38.4) also exits order to understand the intermediate water properties and
Gibraltar in a bottom layer (Tsimplis and Bryden 2000). The pathways. There are two main types of deep water in the
incoming AW is modified by mixing and air-sea fluxes as it Mediterranean: Western Mediterranean Deep Water
traverses the basin, and some of it leaves the surface layer (WMDW) and Eastern Mediterranean Deep Water
through densification in both east and west “closed” over- (EMDW). Each water mass accumulates at depths much
turning cells (relatively cold, salty water sinks in sporadic greater than the sill depths separating the basins from each
events at particular locations to particular depths). The dis- other and the Atlantic. The water masses spread along the
placed deeper waters upwell in much broader, slower pro- bottom, mixing with the surroundings which modifies the
cesses over each basin, then mix with intermediate waters deep layers.
that have formed through less intense densification, which The WMDW forms in the Gulf of Lions nearly every
traverse back to the west in complicated ways. Finally, the February–March after intense surface buoyancy loss (evapo-
uppermost part of this intermediate layer, a form of the LIW, ration and cooling via latent and sensible means) is applied
Fig. 18.3 (a) The

thermohaline of the
Mediterranean in the time
before and after and (b)
during the Eastern
Mediterranean Transient.
(Modified from Tsimplis et al.
2006, figures a and b ©
Daniel Hayes)
to pre-conditioned waters in the open sea. Strong, destabilis- to decadal variability of a “precarious balance” in the source
ing buoyancy loss occurs during occasions with high winds, location of EMDW (Roether et al. 2007). In 1989, deep and
which also mix the surface layer mechanically. If the surface intermediate water from the Cretan Sea (CDW and CIW)
fluxes are strong, frequent and/or long enough for the given were dense enough to sink to the depths of the Levantine for
water column properties, WMDW is produced. If not, an the first time in instrumental records (Theocharis et al. 1999).
intermediate water mass is produced: Western Intermediate Before that, CDW left the Cretan Sea and settled to depths
Water (WIW). The WIW is cooler and fresher than the LIW below the LIW, but above EMDW of Adriatic origin. The
that arrives from the eastern Mediterranean. The presence of formation of EMDW in the Adriatic is influenced by the LIW
AW with salinity higher than normal near the surface and the properties and the dense shelf water of the northern Adriatic
underlying LIW contributes to more efficient production of that cascades along the west coast to mix with the LIW in the
these two types of water, as less buoyancy loss is required to South Adriatic cyclonic gyre. This Adriatic Deep Water
produce a denser water mass. Therefore, as the AW and LIW (ADW) spreads into the depths of the Ionian and Levantine
properties vary, the volume and density of the water mass Seas. In the years from 1989 to 1992, the Cretan Sea domi-
formed varies interannually. In recent years WMDW has nated the formation of EMDW, and this may be explained by
become progressively warmer and saltier (Schroeder et al. an oscillation of the Ionian Circulation which feeds more or
2010; Houpert et al. 2016). Some years the ocean bottom is less LIW into the southern Adriatic (Borzelli et al. 2009;
reached (about 2400 m) and some years lesser depths are Gačić et al. 2010, 2011; Theocharis et al. 2014). Harsh
reached (about 1500 m). Dense water production on the shelf weather conditions in the northern Adriatic can trigger the
can also result in cascading dense water plumes reaching formation and spreading of extremely dense EMDW. See
depths from 200 to 2000 m or more (Canals et al. 2006; Bensi et al. (2013) for an example in 2012. In all cases of
Durrieu de Madron et al. 2005, 2013). deep water formation, the presence and properties of LIW
The EMDW forms either in the southern Adriatic Sea play a critical part (Wu and Haines 1996; Skliris and
(Fig. 18.3a) or the Aegean Sea (Fig. 18.3b). Evidence points Lascaratos 2004).
18.3.3 Levantine Intermediate Water in net evaporation (evaporation minus precipitation, or E-P)
Formation in the whole southern part of the EMED, which significantly
increased between 1990–1999 and 2000–2015 (the sign of
Levantine Intermediate Water (LIW) is usually defined in the the E-P anomaly time series, from 1980 to 2016, switched in
eastern Mediterranean by a potential density anomaly σθ of 1998 from negative to positive). So, a prolonged
28.85–29.10 kg m−3 (temperature of 15–16 °C and salinity intensification of net evaporation is affecting the region
38.95–39.05) (Lascaratos et al. 1993). Taken together, where the eastward pathway of the LSW occurs: this strongly
historical studies (Table 1 of Lascaratos et al. 1993) show modified LSW will later on transform into a saltier and
wider ranges (28.85–29.15, 14.6–16.4 °C, 38.85–39.15); warmer LIW.
LIW resides primarily at depths between 150 and 400 m, The role of LIW is crucial in determining the amount and
although naturally it is found at and near the surface in characteristics of the deep waters (Wu and Haines 1996) that
regions in which it is formed and descends as it spreads to are formed in and ventilate both the EMED and the
other regions. It has been seen as deep as 500 m at the base WMED. These waters are formed with properties that are
of the anticyclonic Cyprus Eddy (Hayes et al. 2016). It can mainly determined by the conditions at surface (air-sea
be seen as a layer of salinity maximum in those depths exchanges) and the hydrographic preconditioning, i.e. heat
throughout the entire Mediterranean, although of different and salt contents, of the surface and intermediate waters that
salinity and temperature because of mixing during its spread contribute to the formation of the deep ones (Schroeder et al.
away from the formation region. 2010). Thus, changes in air-sea fluxes (of heat and
This water mass most likely forms in the Rhodes Gyre freshwater), interior ocean circulation and mixing can alter
(Nielsen 1912; Lacombe and Tchernia 1960; Wüst 1961; the signature of the new deep waters (in terms of T, S,
Ovchinnikov 1984; Schlitzer et al. 1991; Lascaratos and equilibrium depth, volume and layer thickness).
Nittis 1998), although many authors have suggested other
locations (Southern Levantine: Morcos 1972; anticyclonic
eddies: Brenner et al. 1991; Northern Levantine: Sur et al. 18.4 Water Mass Characteristics and Flows
1992; LIWEX Group 2003). Unfortunately, observations are
insufficient to support claims as to the dominance and persis- 18.4.1 Eastern Mediterranean
tence of the various sources. Rare, direct observations were
described in LIWEX Group (2003) when in fact deep water Various mechanisms and locations may generate LIW in the
formation was observed in the Rhodes Gyre. In that study, Eastern Mediterranean in winter, which then spreads
LIW was formed by simple cooling and evaporation of the throughout the basin, eventually leaving through the Sicily
surface mixed layer, which deepened gradually to 100 m. Channel, possibly after one or more circuits in the basin. The
Since direct observations are scarce, various numerical and sill depth at the Sicily Channel is just over 500 m, but the
reanalysis studies have been carried out. In numerical simu- channel is only 35 km wide below 200 m depth. The path this
lations (Lascaratos and Nittis 1998; Nittis and Lascaratos water follows through the basin is not well documented, with
1998), mixing to 400 m was simulated in the Rhodes Gyre, most of the available observations sparsely distributed in
favored because the upward-doming isopycnals of the time and space. These have been supplemented by and
cyclonic gyre reduced the surface density and intermediate compared with numerical simulations, and have been
stability of the water column underlying the mixed layer. incorporated in re-analyses (models that assimilate historical
This is believed to be the primary mechanism for LIW for- data). After formation, lateral (isopycnal) spreading and
mation. A short summary of the above can also be found in mixing occur, modifying the initial T-S properties. Both
Schroeder et al. (2012). mean flow and eddies transport LIW throughout the eastern
A warmer and drier regional climate in the EMED favours basin. In some cases, LIW is a distinct, homogeneous layer
the formation of warmer and saltier intermediate layer, given (thermostad in the core of an eddy), but in other cases it is
that LIW is formed by transformation (densification due to not, and both mean flow and eddy flux can exist at the same
evaporation and cooling) and sinking of Levantine Surface time.
Water (LSW). The LSW originates from the modification of While there are a few early hydrographic studies related to
AW along its path through the Ionian and the Levantine, the formation of deep and intermediate water (see above),
where it becomes particularly warm and salty. Hence the cli- they do not reveal much information on the dispersion path-
matic conditions along this path are likely to be crucial in ways because they do not cover large regions synoptically,
eventually determine the heat and salt content of LIW. In this nor with statistical significance. The intermediate circulation
regard, it is worth noting that Cook et al. (2016) reports a in the eastern Mediterranean was first estimated by
recent drought in the Levant (since 1998) which is the driest Ovchinnikov (1966). Based on hydrographic cruises, he con-
in the past 500 years. Schroeder et al. (2017) show a change cluded that the intermediate circulation is a less-intense ver-
sion of the surface circulation (which cannot be true clonic eddies containing LIW. From 1985 to 1990, dynamic
everywhere and at least not at Sicily and Gibraltar Straits or height maps for each POEM cruise at 300 dbar relative to
there would be no balance with the surface Atlantic Water 800 dbar showed long-lived (months to years) anticyclonic
inflow). Gerges (1977) uses a diagnostic model to conclude eddies intermingled with a weaker cyclonic circulation of the
the intermediate layers of the Levantine Sea move cycloni- Rhodes Gyre.
cally around the basin, as was believed to be the case near the Schlitzer et al. (1991) describe the westward spreading
surface. In that same study, another cyclonic gyre is illus- and modification of LIW away from what appears to be the
trated in the Ionian, while there is a weak exchange at the source region in the northern Levantine from a ship-based
Sicily Channel. Malanotte-Rizzoli and Hecht (1988) sum- tracer and hydrography experiment. Substantial mixing with
marise the state of knowledge before mesoscale effects were water below 500 m is noted, before passing the Sicily
sufficiently observed. Of note is the study of Wüst (1961) Channel. The LIWEX Group (2003), who found that subse-
showing LIW flowing westwards from the formation region quent to Levantine deep and intermediate water mass forma-
(Rhodes Gyre) and mixing with layers above/below. Other tion in the Rhodes Gyre and northern Levantine (respectively),
studies show that the salinity maximum is distinct enough to LIW subducts under the low density layers of the surface and
be observed in the Ionian, the Adriatic, and parts of the west- spreads along isopycnal surfaces. Based on grids of tempera-
ern Mediterranean with a core value of 38.9 at the Cretan ture, salinity, and oxygen profiles, it is claimed that one path-
Passage and 38.7 at the Sicily Channel (Malanotte-Rizzoli way is to the west, into the Aegean and Cretan Seas, with
and Hecht 1988). The dispersion of LIW in the Levantine Sea some of the LIW continuing around the cyclonic gyre, head-
was described in detail for the first time as part of an Israeli ing back east after passing Crete. A second pathway is
cruise program called Marine Climate in the period 1979– directly south from the formation region, opposing the
1984 (Hecht et al. 1988), with the new picture emerging that cyclonic flow of the gyre, and possibly entering an open sea
LIW spatial distribution in the Levantine was correlated with eddy (Fig. 18.4). Attempts to synthesise available hydro-
mesoscale variability, with LIW often trapped inside anticy- graphic observations to estimate LIW pathways were made
clonic eddies. Scales of features resolved were 60–100 km. by Millot and Taupier-Letage (2005a), who show only a few
The fact that mesoscale variability dominated the spreading indicative arrows in the eastern Mediterranean. The only
of LIW within the entire eastern basin was revealed by the suggested direct paths of LIW are the ones from the main
POEM cruises as described by Özsoy et al. (1989, 1991). formation area in the Rhodes Gyre towards the west along
Ozturgut (1976), and Ovchinnikov (1984) also link LIW for- the northern edges of the Cretan Passage and Ionian Seas
mation to mesoscale processes, which prove to be a critical (Millot and Taupier-Letage 2005a). Other pathways of LIW
aspect of the eastern Mediterranean. mentioned in the latter study are the entrainment into wind-
Based on POEM cruises in March of 1989, deep excur- induced eddies along the northern coast (Ierapetra and
sions of the 15 °C isotherm (to 500 m) were shown away Pelops), the entry of some LIW into the southern Adriatic,
from the Rhodes Gyre (Özsoy et al. 1993), while near the and the recirculation at the Sicily Channel.
center of the gyre, very shallow depths of 10 m were All of these studies are affected by the same issue: the
observed. These excursions were associated with anticy- observational data were of limited spatial and temporal
Fig. 18.4 Salinity at

potential density anomaly of
29.0 kg m−3 from the LIWEX
1995 cruise. Orange oval
indicates the region of LIW
formation (Northern
Levantine). Red arrows
indicate likely pathways
based on salinity gradient.
(Adapted from LIWEX group
2003)
extent and spatial resolution was very low. It is very likely There is also an indication of a transport of LIW towards the
that subbasin (30–150 km), mesoscale (10–30 km) and east out of the Rhodes Gyre (Fig. 18.5).
smaller processes are responsible for the spreading of In a recent numerical reanalysis experiment (Pinardi et al.
intermediate water, but were not resolved, or did not occur 2015), the intermediate layer circulation (200–300 m) was
during the short time of the particular cruise. Further studies computed based on a mean of monthly means over the years
have published maps based on model simulations (Wu and 1987–2007 (Fig. 18.6). However, this can be misleading
Haines 1996; Lascaratos and Nittis 1998) and re-analysis since actual transport of LIW can occur against the mean
(Pinardi et al. 2015), which solve the problem of resolution flow due to time varying flow (Stratford and Williams 1997).
and extent, but tend to raise more questions than they answer In addition, flow in the ocean more closely moves along den-
because of the complex eddy fields and decadal variability sity layers, not depth layers. For these reasons, the salinity
revealed. In particular, the model results of Wu and Haines and currents on the 28.95 kg m−3 potential density anomaly
(1996) provide deep insights into the dispersal of LIW surface from the Copernicus Marine Environment Monitoring
throughout the Mediterranean. They find that the LIW Service (CMEMS 2017) daily model re-analysis output are
formed in their model (prescribed in the Rhodes Gyre by also computed here. Averages of instantaneous fields from
surface relaxation) breaks up in baroclinic eddies (stratified every 10 days of 2016 show the spreading of LIW in many
flow instabilities) which can move eastward against the directions away from the south of Crete (Fig. 18.6). This is
direction of mean flow. The net effect of the eddies could be suggested to be the region where LIW was most recently
to transfer LIW north of Cyprus, southward along the coast formed as it has the highest salinities. A branch spreading
of Lebanon and Israel (Plate 3 of Wu and Haines 1996). A eastward along the Turkish coast is evident, as well as
mean flow to the west out of the gyre is also seen (as in previ- branches encircling Cyprus and the region south of the
ous modeling studies that did not resolve eddies such as Rhodes Gyre. In the latter region the LIW seems to encircle
Haines and Wu 1995). This branch enters and leaves the a set of three anticyclones. West of Crete the LIW heads
Aegean, joining the Ionian basin. Some of this branch also straight west into the Ionian, but also with indications of a
recirculates eastward in the Mersa-Matruh Gyre, and possi- branch heading northward into the Adriatic, which is not
bly back to the Rhodes Gyre. The idea of mean and time- shown by Pinardi et al. (2015). An instantaneous image from
varying transports was proven to be valuable in Stratford and 31 January 2016 (Fig. 18.6) indicates the complex transport
Williams (1997), who show that tracers released in the processes via geostrophic turbulence. It is nearly impossible
Rhodes Gyre simulated by the GCM of Wu and Haines to track specific parcels without a separate tracer experiment.
(1996) not only spread westward into the Aegean under the Even if this were done, it is not clear that the model can
mean flow, but that eddy fluxes were required to account for adequately simulate the spreading of LIW. Anti-cyclonic
the flow southward and eastward. This is also described by eddies with a core of LIW have been observed numerous
Lascaratos and Nittis (1998). Additional evidence for LIW times with gliders or profiling floats that were not predicted
pathways can be seen from the 120-year model run of Wu by operational models. In some cases, similar features were
and Haines (1998). By mapping the mean salinity on the only present in the re-analysis because of assimilated data.
LIW density level (28.95 kg m−3) from the last 20 years, it is It is also noted from other studies that the Adriatic Sea
possible to discern one branch exiting the Aegean and mov- also accepts LIW as a sub-surface layer overlaying Adriatic
ing into the Ionian, and eventually the Adriatic, while another water through the Otranto Channel. Over a few years, LIW,
branch moves south out of the Rhodes Gyre, then west along circulating cyclonically in the southern Adriatic,
the southern Mediterranean coast to the Sicily Channel. preconditions the area for deep convection and deep water
Fig. 18.5 Salinity on the

28.95 kg m−3 isopycnal
surface from a 20 year
average after a 100-year
simulation. (Adapted from
Wu and Haines 1998). Orange
oval indicates the region of
LIW formation (Northern
Levantine). Red arrows
indicate likely pathways
based on salinity gradient
Fig. 18.6 (a) Eastern a

Mediterranean intermediate 44.0°N
layer circulation (200–300 m)
from Pinardi et al. (2015). (b)
2016 average salinity and
currents on 28.95 kg m−3 σθ 40.0°N
potential density anomaly
LATITUDE
from CMEMS (2017). (c)
Salinity on same density layer
for 31 January 2016 36.0°N
instantaneous (white areas are
where the isopycnal
outcrops). Generated using
E.U. Copernicus Marine 32.0°N
Service Information
16°E 20°E 24°E 28°E 32°E 36°E

LONGITUDE
b 39.4
39.35
44.0°N
39.3
39.25
39.2
39.15
39.1
39.05
40.0°N
39
38.95
LATITUDE
38.9
38.85
38.8
36.0°N 38.75
38.7
38.65
38.6
38.55
38.5
32.0°N 38.45
38.4
38.35
38.3
16°E 20°E 24°E 28°E 32°E 36°E
UPYC, VPYC 0.400 LONGITUDE
c 39.3
44.0°N 39.25
39.2
39.15
39.1
39.05
40.0°N 39
38.95
LATITUDE
38.9
38.85
38.8
36.0°N 38.75
38.7
38.65
38.6
38.55
32.0°N 38.5
38.45
38.4
16°E 20°E 24°E 28°E 32°E 36°E
LONGITUDE
formation that spills back out into the Mediterranean and By far the most extensive study so far regarding the direct
spreads eastward below existing LIW (Wu and Haines 1996). measurement of the intermediate water circulation in the
Pinardi et al. (2015) do not indicate this current in the sche- Mediterranean is that of Menna and Poulain (2010), who
matic of the intermediate circulation. Further west, it appears used profiling floats to describe the currents at 350 m. They
that the Ionian Sea is split from NW to SE by a front in LIW found that in the Eastern basin, the flow was primarily along
properties. This front generates eddies but is maintained for bathymetric contours at mean speeds of about 5 cm s−1,
many years in Wu and Haines (1996). This would indicate a except in regions of narrow passages. However, this flow was
dynamic barrier to spread of LIW in addition to the topo- also dominated by fluctuation, not steady mean flow.
graphic one further west at the Sicily Channel, although the Recent efforts have been made by the authors to map LIW
latter is likely the rate-limiting one. pathways using hydrographic properties measured from pro-
Fig. 18.7 Map of pressure (dbar) of 29.0 kg m−3 isopycnal from Argo floats from 2002 to 2014, recent years are plotted on top of previous. The
box indicates the region included in the time series (Fig. 18.9). (Modified from Hayes et al. 2014, figures a and b © Daniel Hayes)
filing floats, gliders and ships (Hayes et al. 2014). The float over time and density windows. Cyprus Basin Oceanography
data were collected and made freely available by the (CYBO) cruise data were extracted from 240 to 260 m
International Argo Program and the national programs that depths. This work (Hayes et al. 2014) reveals interannual
contribute to it (http://www.argo.ucsd.edu, http://argo.jcom- variability which has yet to be fully explained: a sudden rise
mops.org). It is part of the Global Ocean Observing System. in temperature and salinity in 2009, followed by a slow
The glider data are available from PANGEA (Hayes 2017). relaxation (Fig. 18.9). Similar variability, using similar data,
From a map of the depth of the LIW isopycnal from such was found by Krokos et al. (2014).
data over the 2002–2015 period, a picture of spreading and Ozer et al. (2017) also showed the thermohaline trends
deepening can be seen (Fig. 18.7). This spreading does not and decadal fluctuation of intermediate water masses in
appear to be the same in all directions, but a series of deep/ south eastern Mediterranean (south of 34°N and east of
shallow variations are visible around the suspected forma- 30°E). They found significant positive trends in both tem-
tion region (Rhodes Gyre). Particularly striking is the depth perature and salinity, along with decadal variability of LIW
of LIW in the Cyprus Eddy, south of Cyprus. This multi-lobe over the years 1979–2014. Prior to this period, and on a lon-
dispersion of LIW in depressed isopycnals is consistent with ger time scale, there is evidence of long-term increasing
the results of Wu and Haines (1996) and Stratford and trends in the LIW core salinity (Rohling and Bryden 1992;
Williams (1997). see Skliris, this volume) as well as sudden shifts (in the
A glider mission through the Rhodes Gyre was recently southeastern Mediterranean; Hecht 1992). An excellent sum-
carried out from 23 March to 5 June 2016 (Hayes 2017). A mary and review of the cross-basin and temporal distribution
pattern of 570 profiles crossing the Rhodes Gyre multiple of nutrients (Dissolved Inorganic Nitrogen (DIN), Total
times was carried out, covering the restratification season Nitrogen (TN), Dissolved Inorganic Phosphorous (DIP),
(March to June). After interpolation, it is possible to see a Total Phosphorous (TP), Total Organic Carbon (TOC)) and
similar lobe-like structure to the LIW surface (Fig. 18.8). oxygen, as well as the carbonate system, is provided by
Besides pathways, the properties of intermediate water reports for the Marine Strategy Framework Directive
are important for studies of CWC. In situ data at intermediate (MSFD) on behalf of the Republic of Cyprus (2012). It is
depths from ships, floats, moorings and gliders can be used shown that the vertically-integrated concentration of nutri-
to track the variability of the LIW temperature and salinity. ents generally decreases from west to east, and at the same
Hydrographic surveys from 1995 to 2012 and recent data time the nutricline deepens. In particular, the phosphacline
from floats and gliders have been used to determine the prop- shows a much stronger deeping (to over 200 m) towards the
erties of LIW in the SE Levantine. For glider and float data, east. The oxygen minimum zone ranges from about 500 m to
the temperature and salinity were extracted and averaged 1000 m and extends deeper with higher concentrations of
Fig. 18.8 Depth of isopycnal

28.8 kg m−3 during
CRELEV-16 glider mission
(23 March to 5 June 2016,
570 profiles). (Source of data
is Hayes 2017)
Fig. 18.9 Time series of (a) salinity and (b) temperature at depth of glider monthly averages with one standard deviation in red dash. Gray
29.0 σθ within the box of Fig. 18.7. Pink: hydrographic cruise averages, dots are float values (not averaged). (Modified from Hayes et al. 2014,
red crosses indicate one standard deviation. Connected blue stars: figures a and b © Daniel Hayes)
oxygen in the eastern as opposed to the western ings occurred (Galil and Zibrowius 1998; Mitchell et al.
Mediterranean. 2013), show a significant change in temperature (16.3–17.2
Time series measurements at 265 dbar from a mooring and back) and salinity (39.21–39.36 and back) over the five
near the Eratosthenes Seamount, close to where CWC sight- months of the experiment (Fig. 18.10). It is surprising to see
Fig. 18.10 (a) Temperature,

(b) salinity, and (c) potential
density from a sensor moored
at 265 dbar southwest of
Cyprus (N33° 53′, E032°
11′), just west of Eratosthenes
Seamount. Bottom depth is
approximately 2650 m. (Data
courtesy CSnet, International,
Inc.)
large excursions in temperature and salinity at this depth, but ancing the inflow of Atlantic Water and the net loss of water
it indicates that the intermediate water is a dynamic water through the upper surface (evaporation-precipitation-
mass in terms of position in the water column and character- runoff).
istics, even away from the formation and coastal areas (the
sea depth is approximately 2650 m in this case.) This is
likely due to the various mechanisms and pathways that 18.4.2 Western Mediterranean
drive the formation and dispersion of LIW, as well as the
decadal variability in the formation of deep waters, which The inflow of fresh surface AW, the evaporation excess over
spread into the basin and mix with the LIW the years after its the basin and strong heat losses during winter in specific
formation. areas, drive an antiestuarine circulation. As the AW spreads
In summary, intermediate water in the Eastern through the basin it is modified: in the eastern Mediterranean
Mediterranean is exclusively represented by various forms of it is transformed into salty and warm LIW. While flowing
LIW, possibly from multiple formation origins. LIW spreads back towards the Western Mediterranean (WMED), it tends
throughout the basin at depths of 0–500 m (normally 200– to gradually lose its characteristics, due to dilution with adja-
350 m). This lateral spreading via large-scale turbulence cent water masses, becoming thus less salty and less warm
seems to be bounded by flow which follows the bathymetric (and less oxygenated due to respiration processes). In addi-
contours cyclonically around the basin. Temperature and tion to these spatial variations, there are also temporal varia-
salinity vary several tenths of degrees and salinity units tions, in particular on the longer time scale. Schroeder et al.
(respectively) on scales of hours up to years according to the (2017) show that since the mid 1990s the temperature (T)
limited in situ observations available. Eventually, LIW exits and the Salinity (S) of the LIW crossing the Sicily Channel,
the Eastern Mediterranean through the Sicily Channel, bal- which divides the EMED and the WMED, have increased by
0.53 °C and 0.13, respectively (i.e. 0.024 °C year−1 and according to (Pinardi et al. 2015) (Fig. 18.11). Broad simi-
0.006 year−1). Such trends are at least one order of magnitude larities to the LIW circulation shown in Millot (1999) and
greater than those reported for the global ocean intermediate many other studies exist: the anticyclonic circulation
layer (Schroeder et al. 2017 and references therein). described above west of Corsica. However, the flow along
Two types of water of eastern Mediterranean origin are the North African coast seems at odds with the circulation of
found in the Sicily Channel: LIW and Aegean and/or Adriatic Millot (1999) and Testor et al. (2005). The salinity and cur-
Deep Water (summarised in Millot 1999). The latter cas- rents on the 28.95 kg m−3 potential density anomaly surface
cades from about 400 m in the Channel to depths of about from the Copernicus Marine Environment Monitoring
2000 m in the Tyrrhenian Sea resulting in Tyrrhenian Dense Service (CMEMS 2017) daily analysis output for 2016 are
Water (TDW) (Millot 1999). The former, LIW, leaves the plotted for the west in the same way as for the east (Fig. 18.11)
Eastern Mediterranean via the Sicily Channel, rounding and also seem to indicate the same anticyclonic circulation
Sardinia to enter the WMEDalong the periphery of the west of Corsica and south of France, but seem to also be at
Tyrrhenian Sea in a cyclonic sense. Properties of the LIW odds with the circulation near the coast of Africa of Pinardi
core in the WMEDare as follows: temperature from 13 to et al. (2015). Averages of the instantaneous 10-day output
14.2 °C, salinity from 38.4 to 38.8, potential density from 29 show good agreement with the schematic Pinardi et al.
to 29.10 kg m−3, and depths from 200 to 600 m (Millot 2013). (2015), with the notable exception of a lack of the westward
The circulation pattern is summarised in Millot (1999) but current along the coast of northern Africa in the simulations.
with caution that turbulence makes such estimates difficult. The simulations show an elongated mean cyclonic circula-
Based on hydrographic studies, Millot (1999) concludes that tion in the western Algerian gyre with strong eastward flow
there is a mean current along the west coast of Italy, which very near the coast in agreement with Testor et al. (2005). As
diverges at Corsica, with some flow north through the Corsica in the eastern basin, instantaneous fields only vaguely resem-
Channel and some making the loop south then back north ble the mean field, indicating that time variable transport
around Sardinia first, then as the Western Corsica Current, could play a significant role and calculating transport based
rejoining downstream of the channel. Once joined, these on mean currents should be done with caution. The instanta-
water masses flow in the Northern Current along the coast of neous image of the salinity at the 28.95 kg m−3 isopycnal
France and Spain. Then, a part flows through the Ibiza again shows complex features, especially in the western
Channel (possibly intermittently), while another part flows Algerian basin and near the Algerian coast. However there
around Menorca. Some LIW exits at Gibraltar, while some are also indications of northward flow along western Sardinia
seems to recirculate eastward, but in an unsteady, turbulent and the continued cyclonic circulation around the basin.
way. Meandering and instability of the eastward current Fabri et al. (2017) show in their study on the Cassidaigne
along the Algerian coast, and the resulting entrainment of canyon and using a habitat suitability model that the living
newer LIW coming from the Sicily Channel into Algerian conditions of CWC communities can be found in areas of the
Eddies were noted by Millot and Taupier-Letage (2005b). canyon where the substratum shows irregularities, slopes and
Testor et al. (2005) has indicated that eddies generated at the topographic highs. Concerning environmental variables
southwest corner of Sardinia (Sardinian Eddies) trap LIW, temperature and high current velocities (with strong
and may transport a significant part of these water masses interactions between the canyon and the along-slope
toward the center of the basin. Northern Current, and wind-induced upwelling) were identi-
An entirely new phenomenon was described by Bosse fied as explanatory factors of the distribution of CWC. Similar
et al. (2015) in which submesoscale vortices of LIW are gen- explanations can be probably drawn for the Catalan canyons
erated west of Corsica and Sardinia and populate the basin, (see Aymà et al., this volume), which are the only ones that
significantly influencing the flux of heat and salt from LIW are regularly impacted by cascading of dense shelf water
vein to the interior. Normally, LIW is considered to play a cascading and storm-induced downwelling, and were rocky
critical role for direct influence of the stability of the Gulf of but also partially sedimented substrates take place. These
Lions and the strength and timing of the formation of canyons are also sites with higher fluxes of organic matter
WMDW in wintertime there. Larger scale eddies have been deriving from the shelf or frontal zones. Along the Catalan
observed previously, Algerian Eddies and Sardinian Eddies, margins, CWCs are found solely in the head of the Lacaze-
but these were limited to the southern sub-basins (Millot and Duthiers, Cap de Creus, and La Fonera canyons. In general,
Taupier-Letage 2005b; Testor and Gascard 2005). According the spotty presence of CWCs is likely a result of local condi-
to Testor et al. (2005) the Algerian basin appears to be char- tions, since LIW borders all of the northern margins of the
acterised by two cyclonic large-scale circulations, which are Mediterranean.
mainly barotropic and have been called the Western and Recently, remarkable changes occurred in the
Eastern Algerian Gyres. WMED. Once advected to the dense water formation region
As for the Eastern Mediterranean (Fig. 18.6), the interme- in the Gulf of Lion (one of the CWC Provinces in Taviani
diate layer circulation of the western Mediterranean is shown et al. 2011), more salt and heat in the LIW will further
Fig. 18.11 (a) Western a

Mediterranean intermediate
layer circulation (200–300) 43.0°N
from Pinardi et al. (2015). (b)
2016 average salinity and 41.0°N
currents on 28.95 kg m−3 σθ
potential density anomaly
39.0°N
from CMEMS (2017). (c)
LATITUDE
Salinity on the same isopycnal
for 21 July 2016 37.0°N
instantaneous (white areas are
where the isopycnal 35.0°N
outcrops). Generated using
E.U. Copernicus Marine
33.0°N
Service Information
31.0°N
6°W 2°W 2°E 6°E 10°E 14°E
LONGITUDE
b 38.9
38.85
43.0°N
38.8
38.75
38.7
41.0°N 38.65
38.6
38.55
39.0°N 38.5
38.45
LATITUDE
38.4
37.0°N 38.35
38.3
38.25
35.0°N 38.2
38.15
38.1
33.0°N 38.05
38
37.95
31.0°N 37.9
6°W 2°W 2°E 6°E 10°E 14°E
UPYC. VPYC 0.400 LONGITUDE
c 38.9
43.0°N 38.85
38.8
38.75
41.0°N 38.7
38.65
38.6
39.0°N 38.55
38.5
LATITUDE
38.45
38.4
37.0°N 38.35
38.3
38.25
35.0°N 38.2
38.15
38.1
38.05
33.0°N 38
37.95
37.9
31.0°N
6°W 2°W 2°E 6°E 10°E 14°E
LONGITUDE
enhance the tendency of this site to produce warmer and et al. 2016), as a consequence of a major DWF event in
saltier deep waters (Schroeder et al. 2010). The homogeneous winter 2004/2005 that set the beginning of the Western
WMDW has long been considered a stable layer to be used Mediterranean Transition (WMT). The WMT is a climate
to quantify gradual trends in T and S possibly induced by shift that radically changed the basic structure and properties
climate change (Schroeder et al. 2016). While deep T and S of the intermediate/deep water column in the western basin:
seem to have increased almost steadily for about half a T, S and density abruptly increased and the weak stratification
century (Rohling and Bryden 1992; Krahmann and Schott has been replaced by a number of vertical gradient inversions.
1998; Bethoux and Gentili 1999; Rixen et al. 2005; Josey The process of formation of large volumes of anomalous
et al. 2011), since 2005 the gradual trend was interrupted by WMDW continued in the following winters (especially in
an abrupt jump towards higher T and S (increasing rates 2005/2006, 2008/2009, 2009/2010, 2010/2011, 2011/2012
were 2.5 times faster than during 1961–2004, see Schroeder and 2012/2013): each winter a new warmer, saltier and
denser deep water formed, leading to a stepwise increase of Brenner S, Rozentraub Z, Bishop J, et al (1991) The mixed-layer/
thermocline cycle of a persistent warm core eddy in the eastern
the heat and the salt contents of the WMDW (Houpert et al. Mediterranean. Dyn Atmos Oceans 15:457–476
2016; Schroeder et al. 2016). These waters will eventually Canals M, Puig P, de Madron XD, et al (2006) Flushing submarine
feed the Mediterranean Outflow Water (MOW) exiting canyons. Nature 444:354
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Acknowledgments Thanks to the reviewers who have pointed out culation of the Mediterranean Sea: water formation and dispersal.
several ways to improve this manuscript. This study has been conducted Oceanol Acta 18:401–417
using E.U. Copernicus Marine Service Information. CSNet Hayes DR (2017) Physical oceanography from nine Seaglider mis-
International, Inc. provided temperature and salinity data. sions in the Mediterranean Sea, Eastern Basin, PANGAEA, https://
doi.org/10.1594/PANGAEA.860867, Supplement to: Hayes DR;
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Mediterranean Sea from 2009 to 2016 as observed from autonomous
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recent scleractinian deep-water corals and coral facies in the east- Aymà A, Aguzzi J, Canals M, et al (this volume) Occurrence of living
ern mediterranean. Facies 57:579–603. https://doi.org/10.1007/ cold-water corals at large depths within submarine canyons of the
s10347-010-0247-8 northwestern Mediterranean Sea
Taviani M, Angeletti L, Canese S, et al (2017) The “Sardinian cold- Evans J, Knittweis L, Borg JA, et al (this volume) Cold water corals in
water coral province” in the context of the Mediterranean coral the Mediterranean: a history of discovery
ecosystems. Deep-Sea Res Part 2 Top Stud Oceanogr 145:61–78. Johnston M, Larsson AI (this volume) Perspectives of biophysical mod-
https://doi.org/10.1016/j.dsr2.2015.12.008 elling with implications on biological connectivity of Mediterranean
Testor P, Gascard J-C (2005) Large scale flow separation and mesoscale cold-water corals
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Testor P, Send U, Gascard J-C, et al (2005) The mean circulation of the past to the future
southwestern Mediterranean Sea: Algerian Gyres. J Geophys Res Taviani M (this volume) Changing views about Mediterranean cold-
110:C11017. https://doi.org/10.1029/2004JC002861 water corals
The LIWEX Group (2003) The Levantine Intermediate Water Vertino A, Taviani M, Coselli C (this volume) Spatio-temporal distribu-
Experiment (LIWEX) Group: Levantine basin—a laboratory for tion of Mediterranean cold-water corals
Occurrence and Biogeography
of Mediterranean Cold-Water Corals 19
Giovanni Chimienti, Marzia Bo, Marco Taviani,
and Francesco Mastrototaro
Abstract scarce knowledge on the Mediterranean deep-sea and on

The term cold-water coral sensu lato groups taxa with a the basin-scale distribution of the most important cold-
more or less pronounced frame-building ability (e.g. water corals species represents crucial biogeographical
Lophelia pertusa and Madrepora oculata) with forest- information. This gives fundamental indications on the
forming organisms both on hard (e.g. Leiopathes glaber- location of the Mediterranean vulnerable deep marine
rima, Parantipathes larix, Callogorgia verticillata and ecosystems for future management strategies.
Viminella flagellum) and soft bottoms (e.g. Isidella elon-
gata, Funiculina quadrangularis and Kophobelemnon Keywords
stelliferum). Cold-water coral species and their occur- Cold-water corals · Hard bottoms · Soft bottoms ·
rence in the Mediterranean Sea are here reviewed and dis- Biogeography · Mediterranean Sea
cussed from a biogeographic point of view, considering
geographical areas of occurrence and bathymetric distri-
bution. The present-day occurrence of living cold-water
corals is then compared to the main deep currents of the 19.1 Introduction
Mediterranean Sea. Due to the proper interaction between
topography and a combination of cold, oxygenated and The deep Mediterranean Sea is inhabited by a variety of cni-
trophic-carrying water masses (i.e. Levantine Intermediate darians distributed on both hard and soft substrata, constitut-
Water, deep waters and cascading effects), cold-water ing in favorable places emblematic ecosystems such as
coral communities develop in a mosaic-like situation ‘white coral’ bioconstructions, antipatharian and soft coral
along the main paths that such water masses follow within ‘animal forests’ (sensu Rossi et al. 2017) or sea pen fields.
the basin. Finally, knowledge gaps and future perspec- The present-day situation is a transient one achieved through
tives in the study of cold-water coral occurrence, distribu- the troubled history of a basin exposed to major geological,
tion and biogeography are highlighted. The currently still climatic and oceanographic vicissitudes in the last million
years (Taviani 2002). A commonly shared view is that the
whole Mediterranean stenoecious fauna was completely
renewed, or at least profoundly reshaped, at the beginning of
the Pliocene (i.e. 5.33 Ma; Manzi et al. 2013) following the
G. Chimienti (*) · F. Mastrototaro deleterious oceanographic conditions imposed by the Late
Dipartimento di Biologia and CoNISMa LRU, Università degli Miocene ‘Messinian Salinity Crisis’ (Por and Dimentman
Studi di Bari Aldo Moro, Bari, Italy 1985; Taviani 2003; Bianchi et al. 2012; Sabelli and Taviani
2014; Freiwald, this volume). Since then, the colonisation of
M. Bo the deep Mediterranean bottoms was served by the Gibraltar
Dipartimento di Scienze della Terra, dell’Ambiente e della Vita,
connection with the Atlantic Ocean, which exclusively con-
Università degli Studi di Genova, Genova, Italy
trols up to present the biogeographic affinity of the basin’s
M. Taviani
bathyal benthos, as documented by the fossil legacy and
present composition (Zibrowius 1980; Raffi and Taviani
1984; Fredj and Laubier 1985; Taviani et al. 2011a, b, this
Woods Hole, MA, USA
volume; Sabelli and Taviani 2014; Vertino et al. 2014, this

https://doi.org/10.1007/978-3-319-91608-8_19
214 G. Chimienti et al.
volume). Besides the function of the relatively shallow groups taxa with a pronounced frame-building ability (e.g. L.
Gibraltar Strait as corridor and filter for potential Atlantic pertusa and M. oculata) with forest-forming organisms both
invaders (Bouchet and Taviani 1992a, b) and/or for on hard (e.g. C. verticillata, V. flagellum and Antipatharia)
Mediterranean migrants (De Mol et al. 2005; Henry et al. and soft substrata (e.g. I. elongata and Pennatulacea). Many
2014), a pivotal role in modeling the present Mediterranean of these species belong to the threatened categories reported
deep water benthos is played by the conspicuous climatic in the IUCN Red List of Mediterranean Anthozoa (Otero
variations which markedly affected this semi-enclosed mid- et al. 2017; Otero and Marin, this volume), i.e. ‘critically
latitude basin in the Plio-Pleistocene (Taviani 2002; Sabelli endangered’ (I. elongata), ‘endangered’ (D. dianthus, L. per-
and Taviani 2014; Vertino et al. 2014; Dubois-Dauphin et al. tusa, M. oculata, L. glaberrima, D. cornigera) and ‘vulner-
2017). able’ (F. quadrangularis). Four species are considered ‘near
The aims of this chapter are twofold. Firstly, we present threatened’ (A. dichotoma, P. larix, C. verticillata, V. flagel-
the distribution of coral life at depths >200 m in the lum) and only one (K. stelliferum) has been categorised as
Mediterranean Sea, by considering not only the scleractinian ‘least concern’ (i.e. not considered to be under any known
settling on hard substrates, but also allied cnidarian assem- threat of extinction now or in the foreseeable future).
blages participating in forming antipatharian and octocoral This heterogeneous ensemble has received attention of
forests, including some colonising soft substrata. Secondly, different quality and quantity, mainly depending on the sub-
we discuss the main biogeographic traits of such taxa. stratum on which the organisms settle. Deep-sea soft bottom
habitats have been historically surveyed much longer than
those of hard bottoms due to being easier to sample (e.g.
19.1.1 Cold-Water Corals Sensu lato using trawls, dredges, grabs and corers). Notwithstanding,
the advances in deep-sea exploration technologies, applied
Cold-water corals (CWCs) have been usually defined as to previously unexplored hard bottoms, have provided in the
deep-water azooxanthellate colonial scleractinian (stony) last decade a wide set of in vivo high quality data about the
corals distributed between ca. 200 and 1200 m (Freiwald presence and distribution of CWCs. As a result, even if their
et al. 2004). Other corals, not necessarily colonial scleractin- exploration only started a few decades ago, deep-sea hard
ians, are also included under the label of CWC (Roberts et al. bottom habitats can be considered much more precisely sur-
2006). From a holistic point of view, CWCs can be regarded veyed and explored with respect to soft bottom ones in terms
as those cold-affinity azooxanthellate cnidarians, usually of visual information and data resolution.
found below 200 m depth in the Mediterranean Sea, many of In the case of soft bottom CWCs, the traditional and
them acting as habitat formers. This wide definition includes destructive methods used to study incoherent substrata pro-
both colonial stony corals building up bioconstructions able vided an extensive and useful amount of presence data at
to persist for long periods of time after the death of the ani- medium/large scale. On the other hand, these methods pro-
mals as well as other sessile cnidarians, mostly anthozoans, vided only weak information about species density, large and
which can live in large aggregations (facies) significantly small-scale distribution and key habitat features. Moreover,
changing the structural heterogeneity of the environment since soft bottoms are affected by trawl fishing, this informa-
where they are settled (Buhl-Mortensen et al. 2010). The dif- tion may be subject to rapid change due to fishing pressures
ferent species fitting with this definition have been here dis- and biological data for soft bottoms need to be updated often.
tinguished for phenotypic sharp features which reflect On the contrary, deep hard bottom CWC habitats are only
taxonomic and ecological differences, both for hard and soft marginally influenced by bottom trawling, but still suffer the
bottom species (Fig. 19.1). On hard bottoms, CWCs are effects of artisanal and recreational fishing activities (e.g.
broadly represented by the white corals Desmophyllum dian- longline) targeting commercial species taking place within
thus (Esper, 1794), Lophelia pertusa (Linnaeus, 1758) and or around these ecosystems (D’Onghia et al. 2003; Orejas
Madrepora oculata Linnaeus, 1758, the black corals et al. 2009; Bo et al. 2014a, 2015; Mytilineou et al. 2014).
Antipathes dichotoma Pallas, 1766, Leiopathes glaberrima These fishing impacts can be either direct (e.g. mechanic
(Esper, 1788) and Parantipathes larix (Esper, 1788), the yel- damage and catches) or indirect (e.g. lost fishing gears).
low coral Dendrophyllia cornigera (Lamarck, 1816), the Despite pristine (i.e. not impacted whatsoever) examples are
alcyonaceans Callogorgia verticillata (Pallas, 1766) and nowadays considered to be very limited in the Mediterranean
Viminella flagellum (Johnson, 1863), and the stylasterid basin (Bo et al. 2015), it is plausible to hypothesise that hard
Errina aspera (Linnaeus, 1767) (Fig. 19.1). The alcyonacean bottoms are, overall, less affected with respect to soft bot-
Isidella elongata (Esper, 1788) and the pennatulaceans toms due to their heterogeneous distribution and relative
Funiculina quadrangularis (Pallas, 1766) and inaccessibility to the most damaging fishing activities.
Kophobelemnon stelliferum (Müller, 1776) represents soft Because of their high ecosystem value, deep CWC habitats
bottom CWCs (Fig. 19.1). Thus, the term CWC as used here (including both those with frame-building corals and coral
19 Occurrence and Biogeography of Mediterranean Cold-Water Corals 215
Fig. 19.1 Hard bottom

CWCs: (a) Desmophyllum
dianthus, (b) Lophelia
pertusa, (c) Madrepora
oculata, (d) Antipathes
dichotoma, (e) Leiopathes
glaberrima, (f) Parantipathes
larix, (g) Dendrophyllia
cornigera, (h) Callogorgia
verticillata, (i) Viminella
flagellum, (j) Errina aspera.
Soft bottom CWCs: (k)
Isidella elongata, (l)
Funiculina quadrangularis,
(m) Kophobelemnon
stelliferum. ((a–c, e, g)
Courtesy of L. Angeletti; (d,
m) modified from Bo et al.
(2011); (f) courtesy of Cau
A., MIPAAF (Montecristo
shoals, Tuscany; 160 m); (h)
modified from Bo et al.
(2014c); (i) courtesy of
MIPAAF, Regione Sardegna
(Porto Corallo, Sardinia;
160 m); (j) modified from
Salvati et al. (2010); (k, l)
modified from Mastrototaro
et al. (2017))
forests) have sparked an exponential interest in the interna- Freiwald 2002; Canals et al. 2006; Orejas et al. 2009; Deidun
tional scientific community and a relevant intensification of et al. 2010; Vertino et al. 2010; Taviani et al. 2011a; Gori
the deep Mediterranean seabed exploration (e.g. Hebbeln et al. 2013; Bo et al. 2015; Grinyó et al. 2016). In the case of
et al. 2009; Orejas et al. 2009; Vertino et al. 2010; Taviani frame-building corals, such localities are currently known as
et al. 2011a; Gori et al. 2013; Savini et al. 2014; Bo et al. CWC provinces.
2015).
By-catch and accidental trawling and artisanal fishing
(e.g. Tursi et al. 2004; Schembri et al. 2007; Deidun et al. 19.2 Mediterranean CWC Occurrences
2010; Mastrototaro et al. 2010; Mytilineou et al. 2014) wryly
revealed numerous Mediterranean coral sites, representing a Areas characterised by a large coral growth and colony den-
starting point for the study of hard bottom CWC habitats dis- sity are recognised as CWC provinces (Taviani et al. 2011a).
tribution. These findings aroused great interest in the scien- The term “province” has been previously used in the north-
tific community in the context of the on-going research on east Atlantic to define large coral mound aggregations devel-
deep coral habitats worldwide, contributing to stimulate the oping in areas of some square kilometers (e.g. Kozachenko
carrying of targeted oceanographic missions in these areas et al. 2002; Wheeler et al. 2005; Huvenne et al. 2005; Henriet
and afterwards in other areas with similar hydrological and et al. 2014). The real biogeographical meaning of the term
morphological features. Occasional and sporadic findings of comes from the Botany, where it defines “a major division of
single specimens or sparse populations of living CWC spe- the biosphere, a phitogeographical subdivision of a region
cies were soon followed by the extraordinary occurrence of characterized by dominand plant species of similar past his-
lush coral sites, with highly structured CWC communities, tory, or a biogeographical zone characterized by a 25–50%
clustered in specific areas where suitable topographic and endemic flora or fauna” (Lincoln and Clark 1998).
oceanographic conditions were simultaneously present (e.g. Considering the increasing discoveries of CWC areas and
Fig. 19.2 Main sectors of the Mediterranean Sea and location of the six CWC provinces described up to date
their importance, the definition of coral province should be Callogorgia verticillata, throughout a wide bathymetric
revisited in the future (Chimienti et al. 2018b). range, from about 450 to 1000 m depth, with a luxuriant
A total of six provinces characterised by the two main coral growth between 500 and 700 m depth (Mastrototaro
framework-forming CWC species, Madrepora oculata and et al. 2010). On the upper part of the mound field, these cor-
Lophelia pertusa, has been identified up to date in the als have been found in mixed aggregations with Dendrophyllia
Mediterranean Sea (Taviani et al. 2017). These CWC prov- cornigera (447–613 m), Antipathes dichotoma (630–640 m)
inces are located, from East to West, in the northern Ionian and Leiopathes glaberrima (200–790 m) (Carlier et al. 2009;
Sea (Santa Maria di Leuca), in the southwestern Adriatic Sea Freiwald et al. 2009; Mastrototaro et al. 2010), while a dense
(Bari Canyon), in the Sicily Channel (South Malta), in the population of the sea pen Kophobelemnon stelliferum has
Sardinia Channel (South Sardinia), in the canyons system of been found from 404 to 467 m depth on the muddy seabed
the Gulf of Lions and in the eastern Alborán Sea (Fig. 19.2). around the mounds, currently representing the largest popu-
A description of each CWC province and its environs is pro- lation of this species ever found in the Mediterranean Sea
vided in the following paragraphs. (Mastrototaro et al. 2013).
Freiwald et al. (2009) reported the occurrence of living M.
oculata (670–744 m), L. pertusa (603–744 m) and D. dian-
19.2.1 Northern Ionian Sea thus about 14 nautical miles (nm) WNW from Santa Maria di
Leuca CWC province, at the Gallipoli escarpment. This
A large CWC province develops patchy over an area of about near-vertical escarpment forming the eastern wall of a major
1000 km2 from 300 to 1100 m depth off Cape Santa Maria di canyon system was characterised by metre-size L. pertusa
Leuca (Ionian Sea, Italy; Fig. 19.2). This province is by far bioconstructions with living corals settled on fossilised coral
the best studied deep-sea area of the Mediterranean Sea and frameworks. Northern Gallipoli, off the Porto Cesareo
the CWC habitat for which most information is available, Marine Protected Area, some living colonies of D. cornigera
having been the subject of many research projects and ocean- have been also observed up to 217 m depth (D’Onghia et al.
ographic missions (e.g. Taviani et al. 2005b, 2011a; Freiwald 2016).
et al. 2009; Mastrototaro et al. 2010; D’Onghia et al. 2012;
Savini et al. 2014). As revealed by acoustic surveys, remotely
operated vehicle (ROV) observations and bottom sampling, 19.2.2 Southern Adriatic Sea
this CWC province is typified by an array of deep-water
coral-rich and coral-poor contexts, or mega-habitats, that The Bari Canyon is an asymmetric East-West oriented two-
provide detritus to bottom sediments, as is usual in CWC branch incision located ca. 16 nm offshore from the city of
banks (Vertino et al. 2010). Bari (southern Adriatic Sea, Italy; Fig. 19.2), and character-
Santa Maria di Leuca CWC province (Fig. 19.3) is popu- ised by sub-vertical flanks in its southern part and less steep
lated by the emblematic stony corals M. oculata, L. pertusa flanks northward. Flanks form a levee complex and evolve
and Desmophyllum dianthus as well as by the alcyonacean basinwards into gentler morphologies at a bathymetric range
Fig. 19.3 Northern Ionian

Sea and southern Adriatic Sea
CWC provinces: (a–e) Santa
Maria di Leuca, (f–i) Bari
Canyon. (a) Fossil
frameworks with living
Madrepora oculata (1),
Desmophyllum dianthus (2)
and sponges (3); (b)
Dendrophyllia cornigera
clusters (4) and M. oculata
(1); (c) white and (d) orange
Lophelia pertusa colonies (5);
(e) M. oculata colonies (1) on
flat bottom. (f) M. oculata
colonies (1) on steep slope;
(g) L. pertusa (5) with sponge
(3); (h) fossil frameworks
colonised by living M.
oculata (1) and sponges (3)
with several sea urchins
Cidaris cidaris (Linnaeus,
1758) (6) and ophiuroids (7);
(i) D. cornigera (4) associated
with sponges (3). ((a–d, f–i)
Modified from Freiwald et al.
(2011); (e) modified from
D’Onghia et al. (2008))
of 200–1700 m (Trincardi et al. 2007; Freiwald et al. 2009; off the Montenegro coast (Angeletti et al. 2014). Here rocky
Angeletti et al. 2014; D’Onghia et al. 2015). Madrepora- blocks, boulders and hardgrounds emerging from the soft
dominated build-ups (Fig. 19.3) develop from 280 to 600 m sediment are colonised at depths of 420–490 m by a con-
depth, with dense aggregations of D. dianthus reported from spicuous CWC assemblage composed of M. oculata, small
490 to 664 m depth (Freiwald et al. 2009, 2011; D’Onghia colonies of L. pertusa, well-developed L. glaberrima colo-
et al. 2015). Lophelia pertusa (306–640 m) and D. cornigera nies, clusters of D. cornigera and patchy dense aggregations
(445–494 m) also occur but are less abundant (Freiwald et al. of C. verticillata. In this area, M. oculata and D. cornigera
2009; Angeletti et al. 2014). have been observed down to 540 m depth (Angeletti et al.
About 26 nm northeast of the Bari Canyon CWC prov- 2014), while fishermen reported some accidental catches by
ince, some CWC growth is present on slumped blocks of the longline of M. oculata and L. glaberrima until 1000 m depth
Gondola slide, with M. oculata between 184 and 372 m depth (D’Onghia et al. 2016). The occurrence of such a rich CWC
and L. pertusa colonising deeper hardgrounds, between 674 community on the southeastern Adriatic margin is significant
and 714 m depth (Freiwald et al. 2009; D’Onghia et al. 2016). for the understanding of the connectivity between discon-
On the other side of the Adriatic Sea, diametrically oppo- tinuous deep-water coral grounds in this sector of the south-
site to the Bari Canyon, another CWC area has been recently ern Adriatic Sea and especially with the Bari Canyon CWC
discovered in a canyon system with depths of down to 400 m province (see also Boavida et al., this volume).
South of Bari Canyon, additional CWC sites have been ulations (i.e. Bari Canyon) with those present in the northern
identified on the Apulian margin, off Monopoli and off the Ionian Sea (i.e. Santa Maria di Leuca) (Taviani et al. 2011a;
Salento peninsula, close to Tricase village. In this last area, Angeletti et al. 2014).
the escarpment is incised by several canyons and with a wide
apron at the base, likely due to slumping from the margin
(Angeletti et al. 2014). The canyon base (720–786 m) is 19.2.3 Sicily Channel
characterised by the presence of blocks colonised by living
D. dianthus as well as by L. pertusa and M. oculata colonies. Live CWCs occur at various sites in the Sicily Channel
Living CWCs also occur southwards, along the Salento pen- between 200 and 1000 m, mainly settling on escarpments,
insula, in the Otranto Strait (778 m), next to the midline seamounts, and the flanks of volcanic islands (Freiwald et al.
between Italy and Albania, where few colonies of the stony 2009). Based upon the accidental collection of live M. ocu-
corals M. oculata and L. pertusa were observed at 775– lata and L. pertusa (Schembri et al. 2007), a CWC province
778 m depth. These recent findings highlight that CWC com- has been defined about 11 nm southwest of Malta (Taviani
munities are much commoner in the southern Adriatic than et al. 2011a, 2015) (Figs. 19.2 and 19.4). This province is
previously supposed, suggesting the presence of an almost characterised by a highly structured CWC community
continuous belt of patchy CWC sites spread along the south- (Deidun et al. 2015). Following a belt dominated by L. gla-
western Italian margin, broadly connecting the Adriatic pop- berrima between 200 and 400 m, the white corals M. ocu-
Fig. 19.4 Sicily Channel and

South Sardinia CWC
provinces: (a–d) South Malta,
(e–h) South Sardinia. (a)
Madrepora oculata
framework (1) and
Callogorgia verticillata (8);
(b) facies of Funiculina
quadrangularis (9); (c) Mixed
aggregation of C. verticillata
(8) parasitised by Savalia
savaglia (10), M. oculata (1),
Lophelia pertusa (5),
Muriceides lepida (11),
Corallium rubrum (12) and
massive sponges (3); (d)
Leiopathes glaberrima forest
(13) with M. oculata (1). (e)
M. oculata frameworks (1);
(f) Mixed M. oculata
framework (1) and
pseudo-reef (2); (g)
framework of M. oculata (1)
with a living specimen of the
deep-sea giant oyster
Neopycnodonte zibrowii (14)
settled on M. oculata (1) and
D. dianthus (2); (h)
Dendrophyllia cornigera (4)
on dead M. oculata rubble.
((a–c) Photo copyright
OCEANA ©LIFE BaĦAR for
N2K; (d) modified from
Freiwald et al. (2011); (e–h)
modified from Taviani et al.
(2017))
lata, L. pertusa and D. dianthus appear at ca. 300 m and then on dead coral frameworks, probably because of high mud
predominate between 390 and 650 m, extending down to sedimentation. Relatively close to this site, M. oculata was
1000 m (Schembri et al. 2007; Freiwald et al. 2009; Knittweis recorded northwest of Sicily, on the Aceste Seamount, and
et al., this volume). In addition, living colonies of D. cornig- D. dianthus off northern Sicily, from Enarete Seamount and
era occur, as well as the calcitic gorgonian Corallium rubrum Filicudi banks (Freiwald et al. 2011).
(Linnaeus, 1758) here reaching its deepest known record of
1016 m (Freiwald et al. 2009; Costantini et al. 2010; Taviani
et al. 2010; Knittweis et al. 2016). Callogorgia verticillata is 19.2.5 Gulf of Lions
present all along the CWC province with the development of
lush gardens from 800 to 1000 m depth (Knittweis et al., this Lush CWC communities are patchy located in the northwest
volume). Active CWC recruitment in the area has been sug- Mediterranean canyons between Cap de Creus and the
gested since 2007 by the occurrence of small L. pertusa colo- Ligurian Sea, in the wide Catalan-Provençal-Ligurian canyon
nies living on a lost fishing line at 622–667 m depth system straddling the Balearic and the Ligurian Sea (Bourcier
(Schembri et al. 2007). On the muddy bottom around the and Zibrowius 1973; Tunesi et al. 2001; Orejas et al. 2009;
coral banks, from 457 to 611 m depth, the community is Gori et al. 2013; Fabri et al. 2014; Fourt et al. 2015, this vol-
dominated by the soft bottom CWC Isidella elongata and ume; Puig and Gili, this volume) (Fig. 19.5). In particular, the
Funiculina quadrangularis (Freiwald et al. 2009). Moreover, Gulf of Lions (Fig. 19.2) is currently considered the core of
a dense L. glaberrima forest, comprising more than 2000 this large province, where CWCs are settled on the vertical
colonies with a maximum density of 4–5 adult colonies m−2, walls of this crescent-shaped continental margin. In this area,
was reported 6 nm off the southwestern coasts of Malta along the continental shelf width reaches a maximum of ca. 70 km
deep (250–400 m) rocky terraces in a marine area exploited and the shelf break is located at ca. 120 m depth, with the slope
by fisheries (Deidun et al. 2015). A rich associated fauna was incised by numerous submarine canyons that extend down to
reported within and in the immediate proximity of the antipa- the continental rise at more than 2000 m depth. The continen-
tharian forest. Some uncommon species such as large clus- tal margin of the Gulf of Lions displays one of the highest
ters of the giant barnacle Pachylasma giganteum (Philippi, canyon densities of the world (Würtz 2012). Cap de Creus and
1836) have been found solely in the South Malta CWC prov- Lacaze-Duthiers canyons represent the westernmost subma-
ince (Schembri et al. 2007). A comprehensive review on the rine canyon system of the Gulf of Lions. Well-developed CWC
associated fauna of the Mediterranean CWC communities is communities have been documented on the rocky flanks of
provided by Rueda et al. (this volume), while Altuna and both canyons (Pérès and Picard 1964; Reyss 1964; Orejas
Poliseno (this volume) offer a comprehensive overview on et al. 2009; Watremez 2012; Gori et al. 2013; Fourt et al. 2014,
the CWC taxonomy. this volume; Puig and Gili, this volume). These communities
Living CWCs are also present at ca. 500–680 m on the are dominated by M. oculata, while L. pertusa and D. cornig-
eastern flank of the Nameless Bank (also called Urania Bank) era are less common, being present as isolated colonies or
and on the southern flank of Linosa island (Freiwald et al. small patches (Orejas et al. 2009; Watremez 2012; Gori et al.
2009) as large colonies of M. oculata and smaller and less 2013). In particular, the population of M. oculata found on the
abundant ones of L. pertusa. Additionally, D. cornigera southern flank of the Cap de Creus canyon seems to comprise
thrived under overhangs (733 m) and in large caves formed one of the denser populations of this species in the
by the volcanic bedrock on the southern slope of the Linosa Mediterranean Sea (Orejas et al. 2009), displaying maximum
Trough (Freiwald et al. 2009). values of around ten colonies m−2, although colony density
data are still scarce within the Mediterranean Sea. On the east-
ern side of the Gulf of Lions, Cassidagne canyon hosts another
19.2.4 South Sardinia and South rich CWC community similar to those of the western canyons
Tyrrhenian Sea (Fabri et al. 2014). The French canyons also host one of the
shallower populations of M. oculata known for the basin so far
A rich CWC site has been recently identified off the southern (180–210 m depth) co-occurring, in an extraordinary assem-
coast of Sardinia (Fig. 19.2), in the Nora canyon, part of the blage, with C. rubrum and Paramuricea clavata (Risso, 1826)
Capo Spartivento canyon system (Taviani et al. 2017). This (Fig. 19.5). Living M. oculata was also found at 280 m depth
area has been named as South Sardinia CWC province, char- during a recent exploration of the easternmost French canyons,
acterised by a flourishing population of M. oculata between in the Ligurian Sea (Fourt et al. 2015). The muddy bottoms
380 and 460 m and by the co-occurrence of D. dianthus, with lying between the canyons of the wide Catalan-Provençal-
only occasional colonies of L. pertusa and D. cornigera Ligurian canyon system host patchy populations of I. elongata
observed at 452 and 440 m, respectively (Taviani et al. 2017) and of the sea pens K. stelliferum and F. quadrangularis, these
(Fig. 19.4). No direct coral growth on hard substrata has two last species sometimes forming mixed aggregations
been reported in this CWC province, where corals grow only between 208 and 270 m (Fabri et al. 2014).
Fig. 19.5 Gulf of Lions and

Alborán Sea CWC provinces:
(a–d) Gulf of Lions, (e–h)
Eastern Alborán Sea. (a)
Madrepora oculata colonies
(1) settled on an oyster reef;
(b) facies of M. oculata (1);
(c) mixed aggregation of M.
oculata (1) and Corallium
rubrum (12); (d) mixed
aggregation of M. oculata (1)
and Paramuricea clavata (15)
with the fish Conger conger
(Linnaeus, 1758) (16). (e)
Aggregation of Lophelia
pertusa (5), Desmophyllum
dianthus (2), Acanthogorgia
hirsuta (17) and other
alcyonaceans on a coral
framework, with the urcin
Cidaris cidaris (6) and the
fishes C. conger (16) and
Helicolenus dactylopterus
(Delaroche, 1809) (18); (f) L.
pertusa (5) on coral
framework with ophiuroids;
(g) coral framework colonised
by L. pertusa (5), D. dianthus
(2), Parantipathes larix (19),
A. hirsuta (17) and other
aclyonacenas, with C. cidaris
(6) and H. dactylopterus (18).
(h) Mixed aggregation of
white corals (e.g. L. pertusa,
(5) and alcyonaceans on dead
coral framework, with H.
dactylopterus (18). ((a, b)
Courtesy of ICM-CSIC/
IFM-GEOMAR; (c, d)
modified from Fabri et al.
(2014); (e–h) modified from
Hebbeln et al. (2009))
19.2.6 Eastern Alborán Sea 432 m). On the soft sediments interspersed with the hard bot-
tom CWC community, local rich aggregations of I. elongata
Hebbeln et al. (2009) reported the first large-scale occur- (303–434 m) and K. stelliferum (reported as K. cf. leuckarti;
rence of CWC assemblages from the Alborán Sea (Fig. 19.2), 303–618 m) are present (Hebbeln et al. 2009). Proceeding
mainly from El Idrissi Bank, the Alborán Ridge and the East southward, the Alborán Ridge hosts the hard bottom CWC L.
Melilla mounds. This latter area is located East of the Spanish pertusa (392–539 m), M. oculata (423–539 m), D. cornigera
city of Melilla, on the Moroccan coast, while the first two (423–426 m) and P. larix (404–407 m), while the surround-
areas lie in the middle between Moroccan and Spanish ing soft bottom is colonised by K. stelliferum (517–602 m)
coasts. El Idrissi bank is characterised by the patchy occur- and by occasional colonies of Pennatula phosphorea
rence of L. pertusa between 387 and 676 m depth and D. Linnaeus, 1758 (570 m). On the East Melilla seamounts,
cornigera between 288 and 465 m, together with forest-like together with L. pertusa (308–365 m), M. oculata (200–
aggregations of L. glaberrima (452–647 m), a thin 360 m), D. cornigera (310 m) and P. larix (296–326 m), the
Parantipathes larix belt (327–382 m) and the occasional solitary coral D. dianthus was found from 308 to 326 m
occurrence of C. verticillata (657 m) and V. flagellum (360– depth (Hebbeln et al. 2009) (Fig. 19.5). Considered collec-
tively, these three areas and some surrounding seamounts represent the only living CWCs in the Mediterranean basin,
(Würtz and Rovere 2015) form a unique CWC province with they have one of the largest bioconstruction capability, pro-
a rich CWC community of both hard and soft bottom, from moting the growth of conspicuous structures (Chimienti
ca. 200 to 680 m depth. et al. 2018b). Desmophyllum dianthus can provide small,
A potential interesting area close to this CWC province is scattered hard substrata on pre-existent coherent substratum
the mound field west of the city of Melilla, a few kilometres and can locally reach high densities (pseudo-colonial bank-
west of the Cape Tres Forcas, along the upper slope of the building species), being usually the faster white coral colo-
Mediterranean Moroccan continental margin, which hosts up nising a substratum as a sort of pioneer CWC (Aymà et al.,
to 103 mounds organised in two main clusters from 299 to this volume; Fourt et al., this volume). The branched stony
590 m depth, with a density of 5 mounds km−2. Although this corals M. oculata and L. pertusa are able to build-up huge
area may represent a promising new CWC site, only fossil frameworks that in certain cases exceed a metre of height
CWC have been found to date (Lo Iacono et al. 2014). and width per colony (e.g. Pardo et al. 2011; Angeletti et al.
Adjoining to the Alborán Sea, an extraordinary shallow 2014; Taviani et al. 2016; Fanelli et al. 2017). The finding of
CWC bank was reported by Álvarez-Pérez et al. (2005) in Madrepora-Lophelia ‘false chimaeras’ (i.e. coral bushes
the Gibraltar Strait, with CWC settled mainly on coarse- made from different CWC species) also revealed the ability
grained sediments. This bank is characterised by Lophelia- of CWC larvae to settle on already established living colo-
dominated frameworks with a preferential depth range of nies of both the same species or a different one (Tursi et al.
150–330 m with M. oculata and E. aspera, as well as the 2004; Arnaud-Haond et al. 2015). CWCs frameworks can
occasional presence of D. dianthus and D. cornigera. Despite remain after the death of the polyps (or the death of a portion
not being very far from the eastern Alborán CWC province of the colony), representing a valuable hard substratum for
(ca. 110 nm), the Gibraltar Strait CWC community can be many associated species (Mastrototaro et al. 2010; Vertino
considered a distinct extra-Mediterranean province because et al. 2010). In fact, the highest α-diversity in CWC grounds
the particular oceanographic conditions, mainly due to the is shown primarily in the dead part of the coral framework
water flowing from the Atlantic Ocean to the and within the proximal sediments (Freiwald and Wilson
MediterraneanSea, give rise to this surprisingly shallow 1998; Roberts et al. 2009b). Thus the ecosystem engineer
occurrence of CWC. role of these corals is expressed especially with the calcare-
ous framework remaining after the partial death of the col-
ony, which allows the settlement of other corals or other
19.3 Hard Bottom CWCs sessile organisms on this calcareous substratum. On a geo-
logical time scale, such high-structured build-ups can pro-
Deep hard bottoms have recently received an increasing duce true carbonate mounds, sometimes encompassing many
attention from the scientific community due to the possibility hundred thousands to millions of years of discontinuous
to find CWC communities. Precipitous (e.g. canyon heads coral succession (Wheeler et al. 2007; Taviani et al. 2011a).
and seamount walls) or rugged (e.g. hardgrounds and Until the advent of deep-sea exploration technologies,
slumped blocks) topographies can be suitable for the settle- CWC frameworks dominated by the so-called white corals
ment of CWCs (Genin et al. 1986; Würtz 2012; Würtz and were considered present in the Mediterranean Sea only as
Rovere 2015) if coupled with certain oceanographic condi- dead loose corals and skeletal remains of a Pleistocenic pros-
tions such as low temperature and enhanced currents, strong perity, afterwards shattered by the emerging oceanographic
enough to prevent burial by deposition of fine sediment and post-glacial conditions (Zibrowius 1980; Delibrias and
to transport food to the coral polyps (Frederiksen et al. 1992; Taviani 1985). Limited initial findings of living white corals
Thiem et al. 2006; Kiriakoulakis et al. 2007). (e.g. Pérès and Picard 1964; Fredj and Laubier 1985; Tunesi
and Diviacco 1997; Taviani et al. 2005a, b) and concomitant
discoveries of true living deep-sea reefs (e.g. Mastrototaro
19.3.1 The White Triad et al. 2002; Schembri et al. 2007) overturned the concept of
extinct (or almost extinct) white corals in the Mediterranean
Among CWCs, many data on presence and distribution Sea (Taviani, this volume) and, currently, at least 37 different
regard the so-called ‘white coral triad’ (Pérès and Picard local occurrences of living CWC belonging to the ‘white
1964; Taviani et al. 2005b), namely the solitary coral D. triad’ have been reported in the literature (Table 19.1;
dianthus as well as the colonial corals Madrepora oculata Fig. 19.6). In particular, the presence of M. oculata and L.
and Lophelia pertusa, this latter recently proposed to be pertusa in the Ionian Sea has been well known since more
revised in Desmophyllum pertusum (Addamo et al. 2015; than a century. The first documented finding of these two
Addamo, this volume). Although these three species do not species in the Mediterranean dates back to the collections
Table 19.1 Occurrence and depth range of CWCs in the Mediterranean Sea
Basin Area ID Depth (m) Species References
Atlantic Gibraltar Strait 1 150–330 D. dianthus Álvarez–Pérez et al. (2005)
Ocean 150–330 L. pertusa
150–330 M. oculata
– D. cornigera
150–330 E. aspera
Alboran Sea Eastern Alboran 2 308–410 D. dianthus Hebbeln et al. (2009), Pardo et al.
CWC province 308–676 L. pertusa (2011), Aguilar et al. (2013),
200–539 M. oculata Maldonado et al. (2013), and Würtz
320–410 A. dichotoma and Rovere (2015)
320–400 A. subpinnata
462–647 L. glaberrima
296–458 P. larix
288–465 D. cornigera
320–657 C. verticillata
90–500 V. flagellum
303–434 I. elongata
303–618 K. stelliferum
Avempace Bank, Los 3 350–400 L. pertusa Ocaña et al. (2000), Pardo et al. (2011),
Olivos Shoal and Off 350–400 M. oculata and Aguilar et al. (2013)
Motril 350–400 A. dichotoma
150–300 F. quadrangularis
Chella Bank 4 243–486 L. pertusa Hebbeln et al. (2009), Pardo et al.
118–486 M. oculata (2011), Lo Iacono et al. (2012), and
300 A. dichotoma Aguilar et al. (2013)
300 P. larix
Balearic Sea Mallorca Channel 5 300–950 D. dianthus Aguilar et al. (2013, 2014), de la
and Emile Baudot – A. dichotoma Torriente et al. (2014), and
Escarpment – L. glaberrima Mastrototaro et al. (2017)
– P. larix
– C. verticillata
Menorca Channel 6 180–330 D. cornigera Gori et al. (2014b), López–González
92–187 A. dichotoma et al. (2015), and Grinyó et al. (2016)
Northeast Menorca 7 301–1163 D. dianthus Montagna et al. (2006)
South Catalonia 8 418–1656 I. elongata Maynou and Cartes (2012) and Cartes
et al. (2013)
La Fonera Canyon 9 130–370 M. oculata Lastras et al. (2016)
(continued)
Gulf of Lions CWC 10 246–541 D. dianthus Bourcier and Zibrowius (1973),
province 180–541 L. pertusa Zibrowius (2003), Orejas et al. (2009),
180–541 M. oculata Fourt and Goujard (2012), Gori et al.
200–210 A. dichotoma (2013), Fabri et al. (2014), and Fourt
et al. (2014, 2015)
200–250 P. larix
Ligurian Sea South-West Nice 11 280 M. oculata Fabri et al. (2014) and Fourt et al.
300 A. dichotoma (2014, 2015)
Off Bergeggi 12 630 M. oculata Gay pers. comm.
(Transylvania wreck)
Vado Ligure Canyon 13 344 L. glaberrima Bo pers. comm.
Mantice Shoal 14 80–120 D. cornigera Bo et al. (2014c)
Gulf of Tigullio 15 212–561 M. oculata Rossi (1958), Tunesi and Diviacco
173–257 F. quadrangularis (1997), and Tunesi et al. (2001)
Santa Lucia Bank 16 140–210 A. subpinnata Bo et al. (2014c)
140–210 A. dichotoma
140–210 P. larix
200 V. flagellum
Off Punta Mesco/ 17 200–560 M. oculata Fanelli et al. (2017)
Levante Canyon
Corsican Sea West Corse 18 100–550 C. verticillata Fourt et al. (2014)
South Corse 19 480 D. dianthus Fourt et al. (2014)
Tyrrhenian Tuscan Archipelago 20 100–200 A. dichotoma Morri et al. (1991) and Bo et al.
Sea 100–200 A. subpinnata (2014b)
150–200 P. larix
Off Civitavecchia 21 – D. dianthus Taviani et al. (2016)
Tavolara Canyon 22 150–280 P. larix Cau pers. comm.
Off Ponza and 23 130–300 A. dichotoma Ingrassia et al. (2016) and Bo pers.
Palmarola 130–300 L. glaberrima comm.
100–220 P. larix
Off Ventotene 24 420 D. dianthus Bortoluzzi pers. comm.
420 L. glaberrima
Palinuro seamount 25 210 L. glaberrima Bo pers. comm.
(continued)
St Eufemia Gulf 26 90–120 A. dichotoma Porporato et al. (2009) and Bo et al.
90–120 P. larix (2012)
Gioia Canyon 27 450 I. elongata Pierdomenico et al. (2016)
450 K. stelliferum
Enarete Seamount 28 – D. dianthus Freiwald et al. (2011)
and Filicudi Bank – D. cornigera
Marco Bank and 29 – M. oculata Freiwald et al. (2011) and Bo et al.
Aceste Seamount 200–250 A. dichotoma (2014c)
260 V. flagellum
Sardinia Sea Asinara Gulf 30 1200 D. dianthus Gay pers. comm.
and Sardinia (Corazzata Roma
Channel wreck)
Southwest Sardinia 31 120–200 A. dichotoma Bo et al. (2015)
115–210 P. larix
South Sardinia 32 380–460 D. dianthus Cau et al. (2015) and Taviani et al.
CWC province 452 L. pertusa (2015)
340 V. flagellum
Sicily Channel Off Pantelleria 33 120–240 V. flagellum Giusti et al. (2012)
Nameless Bank 34 509–604 L. pertusa Freiwald et al. (2009, 2011)
(Urania Bank) 509–613 M. oculata
Linosa Through 35 669–679 L. pertusa Freiwald et al. (2009, 2011)
733 D. cornigera
487 A. dichotoma Angeletti pers. comm.
Lampedusa shoals 36 270 D. cornigera Bo pers. comm.
Gela Basin 37 – D. dianthus Angeletti pers. comm.
– L. pertusa
Malta and South 38 390–617 D. dianthus Schembri et al. (2007), Freiwald et al.
Malta CWC 390–667 L. pertusa (2009), Deidun et al. (2015), Evans
province 200–1000 M. oculata et al. (2016), and Knittweis et al. (this
100–400 A. subpinnata volume)
– D. cornigera
– K. stelliferum
Malta Escarpment 39 310–315 A. dichotoma Angeletti et al. (2015)
(continued)
Ionian Sea Messina Strait 40 90–220 E. aspera Giacobbe (2001), Giacobbe et al.
(2007), and Salvati et al. (2010)
Amendolara Bank 41 120–180 D. cornigera Bo et al. (2014c)
Off Porto Cesareo 42 100–217 D. cornigera D’Onghia et al. (2016)
Gallipoli Escarpment 43 740 D. dianthus Freiwald et al. (2009, 2011)
603–744 L. pertusa
Santa Maria di 44 525–1100 D. dianthus Mastrototaro et al. (2002, 2010, 2013),
Leuca CWC 469–1100 L. pertusa Tursi et al. (2004), Taviani et al.
province 425–1100 M. oculata (2005a, b), Carlier et al. (2009),
630–640 A. dichotoma Freiwald et al. (2009, 2011), Gori et al.
(2014b), Savini et al. (2014), and
D’Onghia et al. (2016)
Northwest Kerkyra 45 496–508 D. dianthus Taviani et al. (2015)
Southwest 46 483–634 D. dianthus Mytilineou et al. (2014)
Cephalonia 516–600 A. dichotoma
Adriatic Sea Tricase and Otranto 47 720–786 D. dianthus Angeletti et al. (2014)
escarpements 720–786 L. pertusa
Off Monopoli 48 558 M. oculata D’Onghia et al. (2016)
Bari Canyon CWC 49 490–664 D. dianthus Freiwald et al. (2009, 2011), Angeletti
province 306–640 L. pertusa et al. (2014), Gori et al. (2014b), and
280–600 M. oculata D’Onghia et al. (2015)
Gondola slide 50 674–714 L. pertusa Freiwald et al. (2009, 2011) and
184–372 M. oculata D’Onghia et al. (2016)
Pomo/Jabuka pits 51 200 F. quadrangularis Martinelli et al. (2013) and Bastari
et al. (2017)
Montenegrian margin 52 420–490 D. dianthus Angeletti et al. (2014), D’Onghia et al.
420–490 L. pertusa (2016), and Angeletti pers. comm.
Aegean Sea South Crete 53 520–620 D. cornigera Smith et al. (2009)
Karpathos 54 600 D. cornigera Gori et al. (2014b)
Chios 55 60–200 C. verticillata Vafidis et al. (1994)
Antipsara 56 420 D. cornigera Gori et al. (2014b)
Kyra Panayia/Mount 57 200–270 D. cornigera Vafidis et al. (1994) and Gori et al.
Athos 60–200 C. verticillata (2014b)
Northwest Lesbos 58 – D. cornigera Vafidis et al. (1994, 1997)
Thassos trough 59 300–350 L. pertusa Vafidis et al. (1997)
Marmara Sea Marmara trough 60 900–1200 D. dianthus Taviani et al. (2011b)
Levantine Sea South Cyprus 61 – D. dianthus Taviani et al. (2016)
ID numbers correspond to those in the maps within the text. CWC provinces are reported in bold
Fig. 19.6 Distribution of the white corals (i.e. Desmophyllum dianthus, Lophelia pertusa and Madrepora oculata) in the Mediterranean Sea.
Numbers refer to the area ID given in Table 19.1
made by the Austrian research ship Pola in 1891 off Santa white corals dredged few years before by Trincardi et al.
Maria di Leuca, where M. oculata and L. pertusa were (2007). Finally, a sixth CWC province was recently docu-
dredged from a depth of 760 m (Steindachner 1891; mented by Taviani et al. (2017) in the Nora Canyon (south-
Marenzeller 1893). Other Mediterranean reports of living ern Sardinia). The six CWC provinces currently recognised
white corals came a century later, from the Ligurian Sea, by have been identified based on the occurrence of the ‘white
Tunesi and Diviacco (1997), while the collection and identi- triad’, with mainly M. oculata-dominated frameworks in
fication of coral by-catch from the eastern Ligurian Sea four of the six provinces (i.e. Bari Canyon, South Malta,
occurred frequently in-between (Orsi-Relini pers. comm.). South Sardinia and Gulf of Lions) and both M. oculata and
Meanwhile, similar single particular observations were made L. pertusa frameworks in the other two (i.e. Santa Maria di
by Reyss (1964) and Bourcier and Zibrowius (1973) in the Leuca and eastern Alborán), while D. dianthus is widespread
Gulf of Lions, as well as by Vafidis et al. (1997) in the Aegean with discrete abundances in all the CWC provinces.
Sea. A remarkable development in CWC exploration history Within the whole Mediterranean Sea, the three white
came in 2000 with the accidental finding of a huge number of coral species are currently known from a bathymetric range
living colonies of M. oculata and L. pertusa between 630 and of 180–1100 m depth, with different ranges for each sub-
1100 m depth during trawl fishing operations again off Cape basin (Fig. 19.7). From the westernmost Alborán Sea and
Santa Maria di Leuca, in the northern Ionian Sea (Mastrototaro the Gibraltar sill to the easternmost Marmara and Cyprus
et al. 2002). This occurrence, expanded by further intentional basins, the Mediterranean is speckled with white corals
coral sampling efforts, provided a large collection of living occurrences except for the African coasts, historically less
CWCs and the precise location of this first discovered CWC explored, from where only the eastern Alborán CWC prov-
province in the Mediterranean Sea (Tursi et al. 2004). The ince is currently known (Fig. 19.6). Madrepora oculata and
finding of another two CWC provinces occurred in 2005 and D. dianthus are usually dominant in shallower areas with
2007 in the Alborán Sea and in the Sicily Channel, respec- respect to L. pertusa (e.g. Mastrototaro et al. 2010; Gori
tively, by Álvarez-Pérez et al. (2005) and Schembri et al. et al. 2013), despite showing almost the same bathymetric
(2007). In the same period, 2006, several CWC sites were range within the basin (Fig. 19.7). This different bathymet-
reported in the Sicily Channel and southern Tyrrhenian Sea ric range of dominance of M. oculata and L. pertusa can be
(Freiwald et al. 2011). The possible presence of a rich CWC due to the physiological differences (e.g. growth rates,
assemblage in the Gulf of Lions canyons system was high- feeding ecology, metabolism, sensitivity to temperature
lighted by Zibrowius (2003) after the observation and the changes, sensitivity to ocean acidification) recently
dredging of white coral colonies, respectively during the assessed from Mediterranean specimens of the two species
cruises CYATOX1 in 1995 and DEPRO96 in 1996. A lush (Orejas et al. 2011; Gori et al. 2014a; Movilla et al. 2014;
CWC assemblage in the area, discovered in 2006, was then Naumann et al. 2014; Reynaud and Ferrier-Pagès, this vol-
described by Orejas et al. (2009). In the same year, the Bari ume). Lophelia pertusa seems to be better adapted to lower
Canyon CWC province was firstly explored by Freiwald temperatures, while M. oculata seems to exhibit a greater
et al. (2009) after the finding of relatively fresh-looking dead ability to grow in warmer waters (Naumann et al. 2014). In
Fig. 19.7 Bathymetric range

of the white corals (a)
Desmophyllum dianthus, (b)
Lophelia pertusa and (c)
Madrepora oculata in the
Mediterranean Sea
fact, an inverse South-North gradient in the relative abun- Bo et al. 2011; Altuna and Poliseno, this volume; Bo and
dance of M. oculata and L. pertusa seems to be present Bavestrello, this volume). Even though this species has never
from the North Atlantic (e.g. the Norwegian shelves) to the been reported to form extremely dense aggregations (0.1 colo-
Mediterranean Sea, with a density increase of M. oculata nies m−2) (Bo et al. 2011, 2012, 2015), it usually co-occurs with
and a decrease of L. pertusa from North to South (Arnaud- other CWCs in multi-specific assemblages (Bo et al. 2011,
Haond et al. 2015). It would be worthwhile to explore the 2012, 2015; Pardo et al. 2011; Mytilineou et al. 2014; Cau et al.
deeper areas of the known Mediterranean CWC provinces 2015, 2017). Leiopathes glaberrima is a tall, arborescent spe-
to assess if dominance by L. pertusa occurs in deeper cies characterised by a branched canopy that may exceed 2 m
waters, as it is the case in the Gulf of Lions canyon system in height and width in the largest specimens (Bo et al. 2015; Bo
(Gori et al. 2013). and Bavestrello, this volume). The species belonging to this
genus are characterised by an extraordinary longevity, being
considered among the oldest-living creatures on Earth (Roark
19.3.2 Black CWCs: Antipatharia et al. 2006). The radiocarbon dating of a Leiopathes colony
from Hawaiian waters revaled an extraordinary age of
Besides white corals, which are the main actors of the currently 4265 years (Roark et al. 2006; Wagner and Opresko 2015) and
defined CWC provinces (Taviani et al. 2011a), there are other Atlanto-Mediterranean L. glaberrima colonies were found to
conspicuous anthozoans that, in the past decades, also proved be as old as 2000 years (Carreiro-Silva et al. 2013; Bo et al.
to be exceptional habitat structuring species. The Mediterranean 2015). Although growth rates vary among individuals and
black coral fauna comprises at least three species that conform depends on locality and depth, the occurrence of millennial
to the criteria defining CWCs in this context – Antipathes specimens was hypothesised to reflect a long-term stability of
dichotoma, Leiopathes glaberrima and Parantipathes larix undisturbed deep biocoenoses, particularly surprising for a
(Fig. 19.1) – even if their depth range usually embraces also a semi-enclosed, heavily exploited basin such as the
large part of the continental shelf above 200 m depth. Antipathes Mediterranean Sea (Bo et al. 2015). Finally, P. larix represents
dichotoma is a large black coral (colonies up to 1.5 m tall and the third black coral species frequently occurring from the shelf
wide) with loose, long, flexible branches. It is currently consid- edge to the bathyal depths in the Mediterranean basin. This
ered a typical Atlanto-Mediterranean species (Opresko 2009; species shows monopodial or sparsely branched colonies up to
Fig. 19.8 Distribution of the black corals (i.e. Antipathes dichotoma, Leiopathes glaberrima and Parantipathes larix) in the Mediterranean Sea.
2 m tall with a characteristic bottlebrush habitus (Bo et al. glaberrima are commonly reported within CWCs provinces
2014b). Both L. glaberrima and P. larix can aggregate in exten- together with frame-building corals (Mastrototaro et al.
sive patches reaching very high densities (4 colonies m−2 and 2010; Freiwald et al. 2011; Pardo et al. 2011; Angeletti et al.
2.5 colonies m−2, respectively for P. larix and L. glaberrima) 2014; Fabri et al. 2014; Deidun et al. 2015).
(Bo et al. 2014b, 2015). They may form mono-specific forests A fourth common black coral species in the Mediterranean
or co-occur with other CWCs (Bo et al. 2014b, 2015; Ingrassia Sea, Antipathella subpinnata (Ellis and Solander, 1786), can
et al. 2016). be occasionally found on deep rocky bottoms down to 600 m
All Mediterranean black corals thrive on hard bottoms, depth (Deidun et al. 2015). However this species is not con-
especially on ridges, terraces and the flanks of canyons and sidered here since its peak of abundance is located within the
seamounts, where they can exploit the currents (Freiwald deep circalittoral zone, between 60 and 150 m depth (Bo
et al. 2009; Bo et al. 2014c, 2015; Angeletti et al. 2015). et al. 2009). Apart from A. subpinnata, which is considered
Nevertheless some records provide evidence of populations to be a Tethyan relict (Bo et al. 2008), the other species have
thriving in heavily silted environments, suggesting a certain numerous congenerics in the nearby Atlantic supporting
tolerance to sedimentation (Bo et al. 2012, 2014c). Habitat their origin from this ocean.
preferences, slow growth rates, late maturity and short larval
dispersal (Miller 1998) are among the principal factors that
may drive the distribution and aggregation patterns of these 19.3.3 Yellow CWCs: Dendrophyllia cornigera
large arborescent anthozoans.
Black corals have been mainly found in the western basin, The so-called yellow and pink corals, i.e. D. cornigera and
mostly in the Sicily Channel, Sardinia Channel, South Dendrophyllia ramea (Linnaeus, 1758), are the most important
Adriatic Sea and Aegean Sea (Fig. 19.8), albeit it is worthy Mediterranean colonial Dendrophylliidae corals (see also
to mention that the eastern basin has been much less explored Altuna and Poliseno, this volume). Originally, they were con-
than the western one. In particular, luxuriant antipatharian sidered by Pérès and Picard (1964) as typical hard bottom coral
forests have been documented for the eastern Alborán Sea species in shallower waters with respect to M. oculata and L.
and the South Malta CWC provinces, southwest Sardinia, pertusa, and these authors’ “offshore deep rock community”
along the Ligurian and Tyrrhenian coasts and off Montenegro was included in the circalittoral zone, unlike the bathyal white
(Table 19.1; Fig. 19.8) (Bo et al. 2009, 2011, 2014b, c, 2015; corals. Pérès and Picard’s view about Dendrophyllia was
Pardo et al. 2011; Angeletti et al. 2014; Deidun et al. 2015; biased by the still imprecise information available, including a
Bo and Bavestrello, this volume; Knittweiss et al., this vol- certain difficulty on how to distinguish these species (Zibrowius
ume). Within the basin, L. glaberrima is widespread from 2003). As shown by Zibrowius (1980), the two Dendrophyllia
120 to 1000 m depth, while A. dichotoma and P. larix show species differ in geographical and depth distribution, and are
an unevenly distribution at 90–645 and 90–460 m depth, not ecologically equivalent. In particular, D. ramea is a shal-
respectively (Table 19.1; Fig. 19.9). In the deeper areas, P. lower species, effectively developing in the circalittoral zone
larix is a more occasional species, while A. dichotoma and L. (e.g. Orejas et al. 2017, this volume), while D. cornigera
Fig. 19.9 Bathymetric
distribution of the black
corals (a) Antipathes
dichotoma, (b) Leiopathes
glaberrima and (c)
Parantipathes larix in the
Mediterranean Sea
reaches greater depths, also colonising the bathyal zone. For peratures are too warm for the other CWC species (Gori
this reason, only D. cornigera is here considered as a CWC et al. 2014b).
coral (Fig. 19.1). This scleractinian coral shows an irregularly Large beds of dead D. cornigera colonies in a natural
branched, rigid morphology and can exceed 30 cm in height. upright and spaced position were reported on the Vercelli
Colonies show typical sulfur-yellow polyps on the top of a Seamount (Central Tyrrhenian Sea; 200 m depth) and the
coral framework anchored on flat or gently sloping hard bot- Marco Bank (northwest Sicily; 200–250 m) (Bo et al. 2014c)
toms, where they usually keep their individuality without form- suggesting that this species may suffer heavy mass mortality
ing complex carbonate frames. Nevertheless, they can occur events due to still unkwnon reasons. Similar situations have
with relatively high densities, as at Mantice Shoal (Ligurian been related to the high hydrothermal activities present in the
Sea, 80–120 m; Bo et al. 2014a) and Amendolara Bank (Ionian Tyrrhenian basin (Bavestrello et al. 2014).
Sea, 120–180 m; Bo pers. comm.), where D. cornigera colo-
nies form dense aggregations on flat muddy bottoms without
any consistent anchorage. 19.3.4 Alcyonacea: Soft CWCs
The currently known distribution of D. cornigera in the on Hard Bottoms
Mediterranean Sea shows this species to be widespread from
the eastern to the western side of the basin (Freiwald et al. Among deep-sea alcyonaceans, the Primnoidae Callogorgia
2009; Orejas et al. 2009; Bo et al. 2011, 2014a, 2015; verticillata and the Ellisellidae Viminella flagellum
Salomidi et al. 2010; Gori et al. 2013; Cau et al. 2015). (Fig. 19.1; see also Altuna and Poliseno, this volume) cur-
However no large monospecific aggregations over 200 m rently represent the most common Mediterranean hard bot-
depth have been found to date in the Mediterranean Sea tom CWC species. Callogorgia verticillata is characterised
(Fig. 19.10). As for the ‘white triad’, this yellow coral occurs by branched feathery fan-like colonies often exceeding 1 m
in all the six CWC provinces identified, with a bathymetric in height and forming dense aggregations. It is an Atlanto-
range of 80–733 m (Table 19.1, Fig. 19.11). Dendrophyllia Mediterranean species with a wide distribution over the
cornigera usually colonises the shallower horizons of CWC entire Atlantic Ocean (Braga-Henriques et al. 2013;
banks, often bathymetrically preceding white and black cor- Bullimore et al. 2013; Locke et al. 2013), as well as within
als. This different bathymetric/distributional range could be the Mediterranean Sea. It has been found in the Alborán
due to the capacity of this species to maintain physiological Sea (Pardo et al. 2011), in the Gulf of Lions (Fabri et al.
functions until 16 °C, resulting in its dominance where tem- 2014), in the Tyrrhenian Sea (Bo et al. 2011, 2012, 2014b,
Fig. 19.10 Distribution of the yellow coral Dendrophyllia cornigera in the Mediterranean Sea. Numbers refer to the area ID given in Table 19.1
distribution of the yellow
coral Dendrophyllia cornigera
in the Mediterranean Sea
2015; Cau et al. 2015, 2017), in the Sicily Channel Giusti et al. 2012). This tall, whip alcyonacean is also an
(Knittweis et al., this volume), in the Ionian Sea (Tursi Atlanto-Mediterranean species, so far reported in the
et al. 2004), in the South Adriatic Sea (Angeletti et al. Mediterranean Sea only from the western basin with rela-
2014) and in the Aegean Sea (Vafidis et al. 1994) tively few records. It seems to have preferences for deep cir-
(Table 19.1; Fig. 19.12). Callogorgia verticillata shows a calittoral hard substrata (from 90 to 200 m depth) where it
wide bathymetric range, from 90 to 1000 m depth, with the forms dense facies (Giusti et al. 2012), although it has been
deepest records in the Sicily Channel and in the Ionian Sea sighted down to 500 m depth (Table 19.1; Fig. 19.13) (Aguilar
(Mastrototaro et al. 2010; Knittweis et al., this volume) et al. 2013). Large facies of V. flagellum are known from
(Fig. 19.13). In particular, C. verticillata has been observed numerous banks and seamounts in the Alborán Sea and
in four of the six identified provinces (i.e. Santa Maria di around the Balearic Islands (Lo Iacono et al. 2012; Aguilar
Leuca, South Malta, Gulf of Lions and eastern Alborán) et al. 2013; Maldonado et al. 2013), along the French can-
usually forming patchily-distributed but locally-dense yons and Corsican coasts (Carpine and Grasshoff 1975; Fourt
aggregations from 400 to 1000 m depth. Important forests and Goujard 2012; Fabri et al. 2014), in the Sicily Channel
have been reported also from shallower sites, such as north- (Giusti et al. 2012), northwest Sicily (Bo et al. 2014c) and
west Sicily (240–280 m) (Bo et al. 2014c) and St Eufemia southern Sardinia (Cau et al. 2015, 2017) (Table 19.1).
Gulf (southern Tyrrhenian Sea; 90–120 m) on flat, heavily Within the Mediterranean basin, large alcyonacean for-
silted hardgrounds (Bo et al. 2012). ests are known from the Gulf of Lions canyon system,
Gardens of C. verticillata are often mixed with other Ligurian and Tyrrhenian Sea, northwest Sardinia, around the
CWC species, creating an extremely heterogeneous and Maltese islands and off Montenegro (Fig. 19.12). From an
three-dimensional habitat (Angeletti et al. 2014). This is also ecological point of view, the large and tall colonies of C.
the case of the less known V. flagellum (Aguilar et al. 2011; verticillata and V. flagellum, as well as those of other arbo-
Fig. 19.12 Distribution of the hard bottom alcyonaceans Callogorgia verticillata and Viminella flagellum in the Mediterranean Sea. Numbers
refer to the area ID given in Table 19.1
range of the alcyonaceans (a)
Callogorgia verticillata and
(b) Viminella flagellum in the
Mediterranean Sea
rescent anthozoans, provide a three-dimensional animal for- 19.3.5 Stylasteridae: The Case of Errina aspera
est to a wide array of small to medium sized species,
especially other alcyonaceans that thrive in these environ- Due to their branched calcareous skeleton, hydroids belong-
ments occasionally forming aggregations, including ing to the Family Stylasteridae are considered habitat-
Acanthogorgia hirsuta Gray, 1857, Swiftia pallida Madsen, forming species (Etnoyer and Morgan 2005). Errina aspera
1970, Bebryce mollis Philippi, 1842, Paramuricea macro- (Fig. 19.1) is the only Stylasteridae species actually found
spina (Koch, 1882), Muriceides lepida Carpine and alive in the Mediterranean Sea (Cairns 1983; Zibrowius and
Grasshoff, 1975, Villogorgia bebrycoides (Koch, 1887) and Cairns 1992; Schuchert 2008; Altuna and Poliseno, this vol-
Placogorgia spp. (Mastrototaro et al. 2010; Freiwald et al. ume). This hydroid can form dense aggregations of branched
2011; Pardo et al. 2011; Bo et al. 2012, 2014c, 2015; Giusti calcareous colonies both in the Atlantic Ocean and in the
et al. 2012; Angeletti et al. 2014; Cau et al. 2015, 2017; Mediterranean Sea (Salvati et al. 2010). Despite E. aspera
Grinyó et al. 2016). has been reported in relatively few Atlantic sites (Zibrowius
and Cairns 1992), it is considered an important component nowadays I. elongata occurs only occasionally in fishing dis-
of deep coral communities (Heifetz 2002). In the card, it is plausible to hypothesise that, given the slow growth
Mediterranean Sea this species is currently found only in the rate of the species, the potential for recovery of the popula-
Messina Strait, at depths between 80 and 230 m (Giacobbe tions is practically nil under continuous fishing pressure.
2001; Giacobbe et al. 2007), where it forms monospecific In spite of the widespread decline of Mediterranean
stands showing exceptionally high densities of about 100 muddy-bottom CWC aggregations, some of these sensitive
colonies m−2 (Salvati et al. 2010). Despite the Messina communities still persist in certain restricted areas. This
Strait’s population is the only one found so far in the mainly happens in areas not accessible to trawling, such as
Mediterranean Sea, other large aggregations of E. aspera near hard bottom coral banks, canyon flanks or accidentally
might occur even deeper in the basin, as it happens in the preserved areas (Mastrototaro et al. 2013, 2015, 2017; Fabri
Gibraltar Strait (Álvarez-Pérez et al. 2005). Peculiar et al. 2014; Bo et al. 2015; Pierdomenico et al. 2016). In fact,
hydrodynamic regimes, as those occurring in strait regions, together with suitable oceanographic and edaphic features,
could be important environmental constraints for this human pressure now also contributes in determining CWCs
species. distribution.
19.4 Soft Bottom CWCs 19.4.1 Isidella elongata
Soft bottom CWCs inhabit extensive regions of the seabed The candelabrum-shaped alcyonacean I. elongata (Fig. 19.1),
thanks to their ability to exploit sedimentary bottoms. Thus, also known as bamboo coral, usually forms dense aggrega-
in theory, such species could take advantage of the exten- tions on Mediterranean bathyal muddy bottoms between 500
sive bathyal muddy bottoms occurring in the Mediterranean and 1650 m depth (and occasionally shallower, up to 115 m
Sea. depth) on relatively flat bottoms with a slope of less than 5%
The massive exploitation of deep-sea benthic habitats (Maurin 1962; Pérès and Picard 1964; Bellan-Santini 1985;
started in the first few decades of the last century with the Maynou and Cartes 2012; Bo et al. 2015; Mastrototaro et al.
relentless development of trawl fishing activities on soft bot- 2017; Altuna and Poliseno, this volume; Rueda et al., this
toms populated by commercial shrimps, such as the red volume). Carpine (1970) reported I. elongata as one of the
shrimps Aristeus antennatus (Risso, 1816) and Aristaeomorpha most common coral species on bathyal soft bottoms in the
foliacea (Risso, 1827) as well as the Norway lobster Nephrops western Mediterranean Sea and, 16 years later, Relini et al.
norvegicus (Linnaeus, 1758). With progress in fishing gear (1986) reported this species as part of the trawling coral
technology, trawling now has a heavy devastating mechanical bycatch. Laubier and Emig (1993) emphasised the ecologi-
impact on deep-sea soft bottom habitats (see also Otero and cal role of I. elongata as a habitat former, as a secondary
Marin, this volume), including bathyal seabeds characterised biological hard substratum for epibiotic species, and as a
by viscous mud with a very fluid superficial layer (normally spawning substratum for the egg masses and eggcases of
occurring at depths between 250 and 500 m) as well as the cephalopods and sharks. Nevertheless, the actual conserva-
firm and compact mud (found at 500–1000 m depth) sensu tion status of this soft bottom CWC is somewhat precarious
Pérès and Picard (1964). Aggregations of the sea pen (GFCM 2009) and it is actually a rare species (Bo et al. 2015;
Funiculina quadrangularis and of the alcyonacean Isidella Mastrototaro et al. 2015, 2017), categorised as critically
elongata, which develop respectively on the two soft bottoms endangered by the IUCN (Otero et al. 2017). Conspicuous
with the above cited edaphic features, almost completely dis- aggregations of I. elongata are currently known from El
appeared from most of the trawlable bottoms of the Idrissi Bank in the eastern Alborán CWC province (Hebbeln
Mediterranean Sea as documented for the Catalan coasts, et al. 2009), in the Mallorca Channel (Mastrototaro et al.
French canyons, Ligurian Sea, Sicily Channel and Ionian Sea 2017), off the southern Catalonian coasts (Maynou and
(D’Onghia et al. 2003; Maynou and Cartes 2012; Cartes et al. Cartes 2012; Cartes et al. 2013), on the soft bottoms inter-
2013; Mastrototaro et al. 2013, 2015; Fabri et al. 2014; Petović spersed in the Gulf of Lions canyon system (Fabri et al.
et al. 2016). Cartes et al. (2013) report the complete extirpa- 2014), in the muddy enclave at the base of the Carloforte
tion of I. elongata from a trawled fishing ground off the Ebro shoal (southwest Sardinia; Bo et al. 2015) and on the muddy
Delta due to a low fishing activity over a period of 15 years. bottoms around the Maltese CWC province (Freiwald et al.
The impact of trawling can be locally accelerated by other 2009), while occasional occurrences have also been reported
fishing practices characterised by high removal rate such as from Greek waters (Mytilineou et al. 2014) (Table 19.1;
longlines (Mytilineou et al. 2014). Considering that this Figs. 19.14 and 19.15). Almost all these known I. elongata
decline was already reported back in 1970s–1980s of the past gardens occur in the immediate proximity of hard coral
century (Arena and Li Greci 1973; Relini et al. 1986) and that banks, canyon systems or rough topographies which protect
Fig. 19.14 Distribution of the soft bottom alcyonacean Isidella elongata in the Mediterranean Sea. Numbers refer to the area ID given in
Table 19.1
distribution of the bamboo
coral Isidella elongata in the
Mediterranean Sea
them from trawling. The only exception is the muddy seabed 2011; Baillon et al. 2012; Mastrototaro et al. 2013; Rueda
of the Mallorca Channel seamounts field where, however, et al., this volume). However, a general picture of these soft
trawling is forbidden because of the occurrence of submarine bottom populations in pristine conditions is still biased by a
electricity cables (Acosta et al. 2004; Mastrototaro et al. reduced number of direct observations, poor knowledge of
2017). The scarce I. elongata sites currently remained in the the ecology and biology of these species, as well as the influ-
Mediterranean Sea (Fig. 19.14), someway protected from ence of the anthropic trawling pressure. Compared to hard
trawling, show high densities due to the marked tendency of bottom aggregations of CWCs, however, those occurring on
this species to form aggregations. mud or on sand seem to respond differently to the constrain-
ing parameters of settling, such as larval dispersal and habi-
tat suitability and the result is a patchy distribution on a large
19.4.2 Pennatulacea scale. Quantitative data on sea pens in the discard from
trawling is variable in this sense, but still always present
Pennatulaceans, most commonly known as sea pens, are (Colloca et al. 2003; Massutí and Reñones 2005; Abad et al.
peculiar colonial octocorals characterised by a more or less 2007; Maynou and Cartes 2012; Mastrototaro et al. 2013;
distinct feather-like appearance and strongly adapted to live Fabri et al. 2014; Chimienti et al. 2015, 2018a). The sea pen
on muddy, sandy or detritic bottoms where they may occa- discard, together with that of other benthic species, moti-
sionally form dense aggregations. Sea pens fields have been vates the creation of Large Marine Protected Areas on soft-
listed as vulnerable marine ecosystems (VMES) and, simi- bottoms (Bastari et al. 2016; Otero and Marin, this volume).
larly to other aggregating anthozoans, they are able to struc- Pennatulaceans often live in moderately high energy envi-
ture the environment and attract vagile fauna (Pardo et al. ronments, as is usual for deep-sea soft bottom species (Gage
Fig. 19.16 Distribution of the deep-sea pennatulaceans Funiculina quadrangularis and Kophobelemnon stelliferum in the Mediterranean Sea.
and Tyler 1991). In the Mediterranean Sea there are at least et al. 2014) and in the Mallorca Channel (Table 19.1;
two major groups of sea pens, separated on the basis of their Fig. 19.17). Further occasional occurrences are in Alborán
main bathymetric distribution. Pennatula rubra (Ellis, 1761), Sea, along the Catalan coasts, French canyons, Gulf of
Veretillum cynomorium (Pallas, 1766) and Pteroeides spino- Naples, South Tyrrhenian and Adriatic Sea (Ocaña et al.
sum (Ellis, 1764) have a preference for the continental shelf 2000; Porporato et al. 2009; Pardo et al. 2011; Bo et al. 2012;
and therefore are not strictly considered CWCs (Gori et al. Aguilar et al. 2013; Cartes et al. 2013; Fabri et al. 2014;
2017). On the contrary, other species such as F. quadrangu- Pierdomenico et al. 2016; Bastari et al. 2018).
laris and Kophobelemnon stelliferum (Fig. 19.1) thrive in the Kophobelemnon stelliferum is considered a cosmopolitan
deepest part of the basin, occasionally forming dense fields species distributed from the Atlantic to the Pacific Ocean
(facies). These species show a wide distribution in the both along the continental shelf and on the slope always on
Mediterranean Sea (Fig. 19.16) from the western to the east- muddy bottoms (Carpine 1970; Ocaña et al. 2000;
ern basins, where an appreciable bottom current is necessary Mastrototaro et al. 2013). This species represents another
mainly for trophic reasons. Thus pennatulaceans are often deep-sea pennatulacean able to form large aggregations as
most common in the more hydrodynamically active areas for example in the Santa Maria di Leuca CWC province at
such as the bases of seamounts, canyon or ridges, slightly depths of 404–467 m (Mastrototaro et al. 2013). This repre-
sloping escarpments and continental slopes (Williams 2011). sents the only Mediterranean facies of K. stelliferum studied
As for I. elongata, deep-sea pennatulacean aggregations so far, while other relevant occurrences are reported in the
are also affected by intense destructive fishing practices and western basin from the eastern Alborán CWC province
the formerly common facies of F. quadrangularis have (300–618 m) to the Gulf of Lions (200–500 m) and the
almost completely disappeared from many Mediterranean southern Tyrrhenian Sea (Gili and Pagès 1987; Ocaña et al.
areas due to trawl fishing (D’Onghia et al. 2003; Sardà et al. 2000; Hebbeln et al. 2009; Pardo et al. 2011; Bo et al. 2012;
2004; Otero and Marin, this volume). Because of its large Fabri et al. 2014; Pierdomenico et al. 2016) (Table 19.1;
size and dense aggregations, F. quadrangularis is often pres- Fig. 19.17).
ent as bycatch although with shrinking abundance (Arena Within the Santa Maria di Leuca K. stelliferum aggrega-
and Li Greci 1973; Relini et al. 1986; Colloca et al. 2003; tion, another deep-sea North Atlantic pennatulacean,
Voultsiadou et al. 2011; Bastari et al. 2018) and it is therefore Protoptilum carpenteri Kölliker, 1872, was found from 240
considered a vulnerable species (Otero et al. 2017; Otero and to 451 m depth. The presence of this rare species is most
Marin, this volume). This whip-like pennatulacean is still probably due to the protection from the trawl fishing offered
locally dominant on the bathyal soft bottom community by hard substrata and coral mounds (Mastrototaro et al.
around the Maltese CWC bank (Freiwald et al. 2009), on the 2015). Perhaps not by chance, the second occurrence of this
muddy bottoms off the Gulf of Tigullio (Ligurian Sea; Tunesi species in the Mediterranean Sea is in another deep-sea
et al. 2001), in the Gulf of Lions Canyon system until the CWC oasis, i.e. the I. elongata facies in the Balearic Sea
Cannes and Var canyons, southwest the city of Nice (Fabri (Mastrototaro et al. 2017).
range of the pennatulaceans
(a) Funiculina
quadrangularis and (b)
Kophobelemnon stelliferum in
the Mediterranean Sea
Pennatula phosphorea Linnaeus, 1758 and Virgularia considered mainly influenced by the Levantine Intermediate
mirabilis (Müller, 1776) represents another two pennatu- Water (LIW), the largest water mass moving in the basin,
lacean species which can occur also in the deep-sea. formed in the northern portion of the eastern Mediterranean
However, they are not considered in the present review and flowing westward (Robinson et al. 2001; Millot and
because no data about consistent habitat-forming aggrega- Taupier-Letage 2005; Hayes et al. this volume). These
tions of these species in the deep-sea are available, to our water masses fill all the CWC sites and provinces of both
best knowledge, in the literature. hard and soft bottoms, and supply food to the corals, facili-
tating also the larva transport and contributing as well to
counteract sedimentation (Fig. 19.18).
19.5 Corals and Currents: A Juxtaposition From the eastern Mediterranean Sea, the LIW mass
flows along the southern continental slope of the Cretan
The occurrence of living CWCs in the Mediterranean Sea arc to the Peloponnesus peninsula, between about 250
does not completely overlap with the findings of subfossil and 600 m depth (Robinson et al. 2001; Manca et al.
CWCs, particularly in the eastern Mediterranean basin (e.g. 2004; Millot and Taupier-Letage 2005). Part of the LIW
Taviani et al. 2011a). Despite the possibility of still undis- reaches the Adriatic Sea and forms a gyre from the Balkan
covered CWC sites, this partial mismatch between living to the Italian coasts while the remaining LIW vein con-
and subfossil CWCs distributions may represents a proxy tinues westward through the Sicily Channel and the
of a dynamic response of these corals to environmental fac- Tyrrhenian Sea.
tors that drive their settlement and that, eventually, deter- Along their entire course, LIW masses are involved in the
mine their demise through time and space (Taviani et al. offshore formation of Mediterranean deep waters, such as
2017). Occurrence, distribution and abundance of CWC the Aegean Deep Water in the eastern Mediterranean, the
species are strongly influenced by several abiotic factors Adriatic Deep Water in the central Mediterranean and the
such as the availability of appropriate substrata, seawater Tyrrhenian Deep Water in the western Mediterranean basin
temperature, oxygen concentration, aragonite saturation (Millot and Taupier-Letage 2005). These dense deep-water
state, water flow regimes and food supply (Frederiksen masses generally follow the circulation of the LIW and con-
et al. 1992; Davies et al. 2008; Dullo et al. 2008; Orejas tribute with oxygen and food supply to the deeper CWC
et al. 2009; Roberts et al. 2009b; Gori et al. 2013). In par- communities. In particular, cold North Adriatic Deep Water
ticular, appropriate currents are considered as one of the (ADW), formed in the shallow northern Adriatic through
main governing factors in CWC distribution, since they cold wind forcing, represents one of the densest water masses
supply corals with food and prevent burial of the corals by in the Mediterranean Sea (Cushman-Roisin et al. 2001). This
sediments (Thiem et al. 2006; Roberts et al. 2009a). water mass flows southward and cascades along the south-
Mediterranean CWCs growth and distribution is currently western margin of the Adriatic sub-basin, proceding south-
Fig. 19.18 Distribution of CWC sites (red dots) and provinces (yellow dots) in the Mediterranean Sea and the main paths of flow of the LIW
(Levantine Intermediate Water) and deep water masses within the basin. (Modified from Taviani et al. 2017)
ward through the Otranto Strait and passing along the Tyrrhenian Sea. Along this path, the Malta CWC province
Apulian Plateau into the Ionian Sea and the Levantine Basin and the other CWC sites benefit from this oxygenated and
(Vilibic and Orlic 2002). The Bari Canyon and the Apulian food-rich water mass flow (Millot and Taupier-Letage 2005)
Adriatic CWC sites are bathed by such dense water masses together with the deep water masses mainly following the
which flow between 400 and 700 m depth (Vilibic and Orlic LIW circulation (Fig. 19.18). Once reaching the northern
2002; Angeletti et al. 2014). LIW and ADW masses seem to Sicily coasts, the LIW mainly circulates cyclonically around
be responsible for the extraordinary CWC growth of the the Tyrrhenian basin, at about 200–600 m depth (Millot and
southern Adriatic Sea, feeding the CWC sites off Montenegro Taupier-Letage 2005). Here, the lush antipatharian gardens
and the ones along the coasts of Apulia, where the two CWC can benefit from a turbulent hydrodynamic regime boosting
provinces of Bari Canyon and Santa Maria di Leuca are pres- their filtering activity and, ultimately, their growth and
ent (Fig. 19.18). Not surprisingly, vigorous coral growth in reproduction.
the Bari Canyon is the best between 300 and 600 m depth In the Tyrrhenian Sea, a LIW vein flows northwards
(Freiwald et al. 2009; D’Onghia et al. 2015). The CWC com- through the Corsica Channel (sill at about 400 m depth)
munity off Montenegro, developing between 420 and 490 m while the remaining LIW flows out through the Sardinia
depth with occasional deeper coral occurrences at 540 m Channel. This LIW mass intercepts the South Sardinia CWC
(Angeletti et al. 2014), also benefits from LIW and partly province together with the deeper Tyrrhenian Deep Water
from the ADW. Considering its recent discovery and that this that outflows into the Algero-Provençal basin, as well as the
CWC site has only been partially explored, it is possible that Western Mediterranean Deep Water flowing eastward
a deeper community supported by the ADW could be pres- (Astraldi et al. 2002). Taviani et al. (2017) report the pres-
ent. The cold, oxygenated and less saline ADW flows through ence of LIW (ca. 200–600 m depth) and cooler and less
the Otranto Channel and moves in geostrophic balance along saline water masses (Tyrrhenian Deep Water and western
the 600–1000 m isobaths through the Santa Maria di Leuca Mediterranean Deep Water, below ca. 600 m depth) bathing
CWC province (Budillon et al. 2010), carrying particulate the South Sardinia CWC community.
matter and nutrients that provide a crucial source for biologi- South of Sardinia, part of the LIW mass can fill the
cal activity in deep waters (De Lazzari et al. 1999; Angeletti Algerian margin and flow towards the central sub-basin,
et al. 2014). In this CWC province, the maximum coral while a second vein flows northwards along the western
growth has been observed between 500 and 700 m depth Sardinia and Corsica slopes, between 250 and 450 m depth
(Freiwald et al. 2009; Budillon et al. 2010). (Gana et al. 2015). This second vein joins with the Corsica
The second LIW branch bypasses the southern Adriatic Channel one, participating in the wintertime formation of
and proceeds westwards along the Calabria-Sicilian margin, deep waters in the Ligurian and the Provençal margin. The
passing through the Sicily Channel and reaching the LIW mass continues along the French and the Spanish slope
and most of it outflows through the Gibraltar Strait, while the White et al. 2005, 2007; Dorschel et al. 2007; Mienis et al.
remainder that bypasses the Strait can continue along the 2007; Orejas et al. 2009). A similar relation has been evi-
North Africa slope. In this way, the CWC provinces of the denced for non-scleractinian CWCs, highlighting the close
Gulf of Lions and the eastern Alborán Sea can benefit from connection between deep corals and turbulent hydrodynamic
food and oxygen carried by the LIW masses, together with regimes (Genin et al. 1986; Bo et al. 2014b). New investiga-
the other CWC sites unevenly distributed along the path of tions along canyons, ridges and seamounts, possibly at
the LIW (Fig. 19.18). deeper depths, would enhance our knowledge on CWC com-
Some of the canyons featuring the Gulf of Lions seabed munities and of their biogeography as modulated by local
are also affected by periodic arrivals of dense shelf water environmental constraints. This will help to optimise habitat
cascades during wintertime (Durrieu de Madron et al. 2005; models predicting the location of new provinces mainly
Canals et al. 2006; Palanques et al. 2006; Puig et al. 2008; based on the seabed topography and hydrodynamic condi-
Puig and Gili, this volume). These cascading events act as a tions. Even more crucial would be the exploration of the
significant natural carbon sequestration and deep-sea ecosys- environs of the currently known CWC sites, possibly explor-
tem fueling mechanism by carrying dissolved and particulate ing them deeper than at present and using high-performing
organic matter to the deep-sea through cold shelf waters and equipment such as workclass ROVs (i.e. multitasking ROVs
supporting the large CWC province living in the area (Canals able to reach depth of some thousand of metres). This could
et al. 2006; Orejas et al. 2009). Moreover, this cascading cold help to the potential discovery of other continuous CWC
water mass is responsible for reduced sediment accumula- belts, as it has been the case along the Apulian margin
tion rates that fully fits with CWC settlement and develop- (Angeletti et al. 2014).
ment (White et al. 2005). Deep soft bottoms have been studied for a longer time
Thanks to the interaction between topography and a com- with respect to hard ones but, paradoxically, they are those
bination of cold, oxygenated and food-carrying water masses for which the least is known, especially in terms of coral
(i.e. LIW, deep waters and cascading effects), CWC com- occurrence and distribution. Knowledge gaps are probably
munities broadly develop in a mosaic-like situation on both linked to the scarce employment of direct visual techniques
hard and soft bottoms along the main path followed by the on muddy areas (e.g. ROVs), the low taxonomic resolution
LIW within the basin (Fig. 19.18), as already highlighted for in the identification of macro and megabenthic species, the
the white corals sites (e.g. Taviani et al. 2017). Few excep- high degree of impact on soft bottoms as well as the overall
tions include localised hydrodynamic features, as for exam- limited scientific exploitment of invertebrate bycatch data on
ple the case of Errina aspera in the Messina Strait. In this different temporal and geographic scales (Chimienti et al.
area, the upwelling of the LIW masses through the E. aspera 2015, 2018a; Petović et al. 2016; Terribile et al. 2015; Altuna
aggregation explains this peculiar occurrence (Giacobbe and Poliseno, this volume; Rueda et al., this volume). On
et al. 2007). Despite the presence of suitable substrata for the bathyal soft bottoms, untrawled areas can hosts pristine or
setting of E. aspera in closeby areas, this stylasterid has not low-impacted CWC communities (e.g. Bo et al. 2015;
been observed where the Messina Strait LIW upwelling does Mastrototaro et al. 2017) whose study could increase our
not operate (Giacobbe 2001). knowledge of their ecological features. This will also pro-
vide the opportunity to understand if and how these commu-
nities respond differently to environmental constraints with
19.6 Knowledge Gaps respect to stressed communities, and which factors drive
aggregation patterns.
The last two decades represented an extraordinary turning A greater attention to the benthic bycatch from fisheries
point for the investigation of the deep Mediterranean habi- would result in more information on the occurrence of new
tats, completely changing our perspective on deep-sea biodi- species, rare species, as well as species (such as antipathari-
versity. ROV footage contributed to giving a visual identity ans, pennatulaceans or alcyonaceans) becaming rare over a
to the assemblages that were listed and partially character- certain temporal scale. The removal rates, together with
ised in the first bionomic efforts (e.g. Pérès and Picard 1964). detailed studies on benthos taxonomy, ecology and biology,
Despite the large sampling effort carried out, a lot still needs would be exceptionally relevant to quantify the populations
to be done and information is still discontinuous and and their distribution. This will also help to define specific
unevenly available within the Mediterranean Sea. Future Mediterranean guidelines to preserve deep-water animal for-
perspectives in researching CWC biogeography may con- ests, for example through the implementation of Deep-Sea
cern the individuation and the exploration of other potential Fishery Restricted Areas (see Otero and Marin, this volume).
CWC sites along the LIW main pathway (Fig. 19.18). The establishment of such areas would present a unique
Scleractinians occur in areas where the interaction between opportunity to evaluate the recovery potential, rate and pat-
currents and topography can generate high-speed flow (e.g. terns of deep-water communities (Tudela et al. 2004).
The filling of knowledge gaps on the affinity of the deep della bordura settentrionale dei banchi della soglia Siculo-Tunisina.
Quad Lab Tecnol Pesca 1:157–201
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well as on population genetics and larval dispersal abilities, lars” of cold-water coral reefs along Atlantic European margins:
would contribute towards understanding the biogeography of prevalent association of Madrepora oculata with Lophelia pertusa,
the Mediterranean CWCs. from reef to colony scale. Deep-Sea Res Part 2 Top Stud Oceanogr
145:110–119. https://doi.org/10.1016/j.dsr2.2015.07.013
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Oceanogr Res Pap 49:1321–1340 sity of Mediterranean deep-sea corals and cold-water corals
Voultsiadou E, Fryganiotis C, Porra M, et al (2011) Diversity of inver- Aymà A, Aguzzi J, Canals M, et al (this volume) Occurrence of living
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Drop Chapter
Gorgonian and Black Coral 20
Assemblages in Deep Coastal Bottoms
and Continental Shelves
of the Mediterranean Sea
Andrea Gori, Jordi Grinyó, Carlos Dominguez-Carrió,

Stefano Ambroso, Pablo J. López-González, Josep-
Maria Gili, Giorgio Bavestrello, and Marzia Bo
Abstract
Coral gardens are increasingly being reported at 40–200 m resulting in a significant rise in the scientific exploration of
depth in the Mediterranean Sea. These coral assemblages deep-sea Mediterranean environments by means of visual
are composed of gorgonians from shallow coastal rocky methods. Such studies have revealed the presence of dense
bottoms extending their distribution to deeper areas, as and highly diverse coral gardens composed by gorgonians
well as by gorgonians and black corals with distribution and black corals in several locations of the Mediterranean
restricted to the continental shelf and upper slope. Sea, from 40 to 200 m depth (Fig. 20.1; Grinyó et al. 2016;
Gorgonians and black corals are among the main struc- Gori et al. 2017; Altuna and Poliseno, this volume). These
tural species in deep benthic ecosystems, providing shelter branching organisms are among the main ecosystem engi-
and reproductive grounds for a highly diverse associated neers (sensu Jones et al. 1994) in deep Mediterranean ben-
fauna. Due to their branching morphology and erect posi- thic communities, generating complex three-dimensional
tion, these deep coral gardens are extremely vulnerable to frameworks that enhance the spatial heterogeneity of the sea-
several fishing activities (bottom trawling, long-lines and bed, favouring a highly diverse associated fauna (Bo et al.
trammel net fishing) and should consequently be protected 2012, 2015; Rueda et al., this volume). Furthermore, by cap-
through an ecosystem-based fishery management. turing plankton and particulate organic matter suspended in
the water, gorgonians and black corals play an important
ecological role in the benthic-pelagic coupling, determining
Keywords a significant flow of matter and energy from the pelagic to
Gorgonians · Black corals · Deep-coastal bottoms · the benthic system (Gili and Coma 1998; Rossi et al. 2017;
Continental shelf · Mediterranean Sea Reynaud and Ferrier-Pagès, this volume).
Gorgonian species typically inhabiting Mediterranean
shallow coastal rocky bottoms above 40 m depth (Eunicella
Technological development has recently increased the acces- singularis, E. cavolinii, Leptogorgia sarmentosa,
sibility of technical diving, remotely operated vehicles Paramuricea clavata and Corallium rubrum) can extend
(ROV) and manned submersibles to ecological research, their bathymetric distribution to deeper coastal areas and the
continental shelf (approx. 40–130 m depth) (Bo et al. 2008;
A. Gori (*) · J. Grinyó · C. Dominguez-Carrió · S. Ambroso
Rossi et al. 2008; Cerrano et al. 2010; Gori et al. 2011;
J.-M. Gili Angiolillo et al. 2016; Grinyó et al. 2016) (Fig. 20.2).
Institut de Ciències del Mar, Consejo Superior de Investigaciones Similarly, E. cavolinii and P. clavata have been reported
Científicas, Barcelona, Spain forming dense populations at similar depths on top of
Mediterranean seamounts (70–100 m depth) (Bo et al. 2011).
P. J. López-González On the continental shelf, the gorgonian Paramuricea
Biodiversidad y Ecología de Invertebrados Marinos, Departamento
de Zoología, Facultad de Biología, Universidad de Sevilla,
macrospina forms extensive populations on maërl beds
Sevilla, Spain (Grinyó et al. 2016) and rocky outcrops (Bo et al. 2012) from
G. Bavestrello · M. Bo
65 to 130 m depth (Fig. 20.2) (see also chapter by Chimienti
Dipartimento di Scienze della Terra, dell’Ambiente e della Vita, et al., this volume and by Altuna and Poliseno, this volume).
Università degli Studi di Genova, Genova, Italy This species has also been observed on shallow-water rocky
https://doi.org/10.1007/978-3-319-91608-8_20
246 A. Gori et al.
Fig. 20.1 Deep coral garden composed of Eunicella cavolinii, green dots are the laser beams, which are 50 cm apart. (Photo credits:
Acanthogorgia hirsuta and Paramuricea macrospina at 160 m depth ICM-CSIC and IFM-GEOMAR)
near Cap Formentor (Menorca Channel, Western Mediterranean Sea),
V. bebrycoides
A. subpinnata
P. macrospina *
A. dichotoma
L. glaberrima
C. verticillata
*
E. singularis
distribution of Mediterranean *
I. elongata
E. cavolinii
C. rubrum
A. hirsuta
P. clavata
S. pallida
gorgonian and black coral
B. mollis
P. larix
species in coastal bottoms and
continental shelf of the
gorgonians black corals
Mediterranean Sea (based on
0
the literature reviewed in Gori
et al. 2017); * precious coral,
** bamboo coral
40
50
Depth (m)
100
150
200
bottoms under the particular hydrodynamic conditions of the ments sustain maximum diversity and abundance of
Sea of Marmara (Vafidis et al. 1994; Topçu and Öztürk Mediterranean gorgonians (Bo et al. 2015; Grinyó et al.
2015). Additionally, it was reported associated to cold-water 2016; Cau et al. 2017; Altuna and Poliseno, this volume).
corals (CWC) at 540–830 m depth (Mastrototaro et al. 2010; Indeed, up to ten species of gorgonians (P. clavata, P. macro-
Vertino et al. 2010; Chimienti et al., this volume), whether spina, E. cavolinii, C. rubrum, Villogorgia bebrycoides,
these records should be confirmed by examination of speci- Acanthogorgia hirsuta, Callogorgia verticillata, Swiftia pal-
mens. Recent studies have shown that shelf edge environ- lida, Viminella flagellum and Bebryce mollis) generate high
20 Gorgonians and Black Corals in Deep Coastal Bottoms and Continental Shelves 247
complex coral gardens on rocky bottoms located at Mediterranean gorgonians and black corals (Linares et al.
100–200 m depth in the Menorca Channel (Grinyó et al. 2007; Bo et al. 2015; Bramanti et al., this volume; Lartaud
2016), the Montecristo Shoals (Bo et al. 2014a) as well as et al., this volume). For this reason, the conservation of deep
along the South Sardinia continental margin (Bo et al. 2015; benthic communities in coastal and off-shore areas should be
Cau et al. 2015, 2017) (Fig. 20.2) (see also Chimienti et al., accomplished through an ecosystem-based management
this volume). High gorgonian diversity on the shelf edge approach (Fabri et al. 2014; Otero and Marin, this volume).
could result from the merging of species with shallower and
deeper distributions, causing a mid-domain effect (Colwell
and Lees 2000; Grinyó et al. 2016). Black corals (Antipathella References
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Drop Chapter
Mediterranean Black Coral 21
Communities
Marzia Bo and Giorgio Bavestrello
Abstract morphologies, but typically they have an arborescent or fla-

Remotely operated vehicle (ROV) investigations of the bellate appearance (Altuna and Poliseno, this volume).
Mediterranean deep continental shelf and bathyal zone Antipatharians are among the most enigmatic anthozoans
have provided, in the last decade, a large amount of data of the Mediterranean basin. Despite they have been known
concerning an enigmatic group of anthozoans: the black for centuries due to occasional fishermen bycatch and most
corals. Taxonomic investigations as well as ecological of them have been described over 200 years ago, the species
and biological studies contributed to unveil the diversity, belonging to this group have always been poorly studied in
population structure, environmental preferences, bathy- this region (Bo et al., in press). During the last decade, the
metric and geographical distribution of these corals. ecological aspects of these anthozoans have been progres-
Remotely operated vehicle footage and accidental bycatch sively revealed and recent explorations have highlighted
data have provided evidences of large impact by fishing their capability of forming large forests (Bo et al. 2008,
activities on the Mediterranean black coral forests such 2012a, 2014a, 2018).
that today, due also to their important ecological role as Four species of black corals have been described as stable
structuring species, they are considered part of vulnerable components of the Mediterranean fauna (Opresko and
marine ecosystems and conservation strategies need to be Försterra 2004): Antipathes dichotoma Pallas, 1766, (Family
developed targeting their protection. Antipathidae), Parantipathes larix (Esper, 1790) (Family
Schizopathidae), Leiopathes glaberrima (Esper, 1792)
Keywords (Family Leiopathidae), and Antipathella subpinnata (Ellis
Antipatharia · CWCs · Animal forests · Habitat-forming and Solander, 1786) (Family Myriopathidae) (Fig. 21.1).
species · Mediterranean Sea Additionally, there is Antipathes fragilis Gravier, 1918
whose type species was lost and its taxonomic position is
highly dubious. A sixth species has recently been found once
Antipatharians, commonly known as black corals due to in the Gibraltar area, Antipathella wollastoni (Gray, 1857),
their dark, chitinous skeleton, constitute a small order of however, this black coral is far more common in the Atlantic
colonial anthozoans (approximately 240 species) showing a basin (Ocaña et al. 2007). Finally, recent deep explorations
wide geographical and bathymetrical distribution (Wagner are revealing new Atlantic entrances in the westernmost
et al. 2012; Altuna and Poliseno, this volume). Known to areas of the Mediterranean basin that are currently under
form very rich communities in shallow-water tropical reefs taxonomic investigation (Bo et al., in press).
(Tazioli et al. 2007), they also occur in deep waters, from the Thanks to deep explorations, black corals, once consid-
circalittoral zone to the abyssal plains, in polar and temper- ered rare species, have been extensively recorded in the
ate regions (Pax et al. 1987; Opresko 2002; Opresko and Alborán Sea, in the whole western basin, in the Sicily
Sanchez 2005; Tazioli et al. 2007; Bo et al. 2018; Chimienti Channel and in the Aegean Sea, with L. glaberrima being the
et al., this volume). Characterised by six-tentacles polyps only one, so far, reported for the most extreme Levantine
and a spiny skeleton, they display a very wide range of corallum basin (Bo et al. 2008, 2018; Altuna and Poliseno, this vol-
ume; Chimienti et al., this volume). Particularly abundant
M. Bo (*) · G. Bavestrello along the continental shelf break, where they form mono or
Dipartimento di Scienze della Terra, dell’Ambiente e della Vita, multispecific forests together with sponges and gorgonians,
Università degli Studi di Genova, Genova, Italy they are found also along the upper bathyal slope and mixed

https://doi.org/10.1007/978-3-319-91608-8_21
250 M. Bo and G. Bavestrello
Fig. 21.1 Most common

Mediterranean black corals.
(a) Circa-littoral mixed
assemblage of Antipathella
subpinnata and Paramuricea
clavata (Favazzina shoals,
Calabria, 70 m); (b) The
commercial species Zeus
faber moving in a black coral
and gorgonian mixed
assemblage (Favazzina shoals,
Calabria, 70 m); (c–e)
Branched colonies of
Antipathes dichotoma and
bottle-brush colonies of
Parantipathes larix in a roche
du large ecosystem (St.
Eufemia Gulf, 120 m); (f)
Branched ramifications of
Leiopathes glaberrima as
refuge for crabs and nursery
for catsharks’ eggs
(Carloforte Shoal, 200 m);
(g–h) Evidences of fishing
impact on colonies of L.
glaberrima (Montecristo
shoals, 200 m and Ponza
Island, 300 m)
with reef building cold-water corals (CWCs) (Bo et al. 2009, 1980s in Malta (Deidun et al. 2010), the major anthropic
2012b; Mastrototaro et al. 2010; Fabri and Pedel 2012; Fabri impact they suffer is the fishing impact, particularly artisanal
et al. 2014; Angeletti et al. 2014). Occasional records have and recreational activities carried out by means of nets and
been made below 1000 m depth (Fabri and Pedel 2012). longlines on deep rocky shoals; in addition, bottom trawling
From an ecological point of view, they can be considered has been hypothesised to have indirect impacts on hard bot-
one of the dominant structuring components of the tom communities due to the resuspension of silt (Bo et al.
Mediterranean animal forests between shallow-water gorgo- 2014b, 2018). Various evidences suggest that black corals,
nian assemblages and deep-water reefs (Bo et al. 2018). This due to their arborescent morphology and their occurrence in
situation is particularly well represented along the Italian dense aggregations, are highly catchable by means of bottom
continental shelf. The coral canopy formed by these species, fishing gears operating on hardgrounds and therefore are
commonly exceeding two meters high, is an optimal refuge among the most common components of fishermen bycatch
for a rich associated sessile and vagile fauna, occasionally (Mytilineou et al. 2014; Otero and Marin, this volume). A
spending here also the reproductive phases of their life cycles large number of populations can be considered greatly
(Gaino et al. 2013). Excluding some sporadic cases of com- impacted such that the picture we have today of their distri-
mercial employment for the jewelry trade reported in the bution might have suffered a great change.
21 Mediterranean Black Coral Communities 251
Due to their role of ecosystem engineers, their slow Bo M, Bavestrello G, Angiolillo M, et al (2018) Persistence of pristine
deep-sea coral gardens in the Mediterranean Sea (SW Sardinia).
growth rates, their great longevity and slow recovery ability PLoS One 10:e0119393
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fishermen and students that contributed to expand our knowledge on experimental long line fishing. Deep-Sea Res Part 2 Top Stud
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for the Environment Land and Sea, Italian Ministry of Agricultural, Opresko DM (2002) Revision of the Antipatharia (Cnidaria: Anthozoa).
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Bo M, Canese S, Bavestrello G (2014a) Discovering Mediterranean
Altuna A, Poliseno A (this volume) Taxonomy, genetics and biodiver-
black coral forests: Parantipathes larix (Anthozoa: Hexacorallia) in
sity of Mediterranean deep-sea corals and cold-water corals
the Tuscan Archipelago, Italy. Ital J Zool 81:112–125
Bo M, Bava S, Canese S, et al (2014b) Fishing impact on deep
Mediterranean rocky habitats as revealed by ROV investigation.
Biol Conserv 171:167–176
Drop Chapter
Recent Discoveries of Extensive Cold- 22
Water Coral Assemblages in Maltese
Waters
Leyla Knittweis, Julian Evans, Ricardo Aguilar,

Helena Álvarez, Joseph A. Borg, Silvia García,
and Patrick J. Schembri
Abstract http://lifebahar.org.mt). The surveys were carried out within

Recent deep-water remotely operated vehicle surveys the 25-nautical mile Fisheries Management Zone (Fig. 22.1a)
around the Maltese Islands resulted in the discovery of around the Maltese Islands, and mostly focused on previ-
highly diverse habitats, including extensive hard bottom ously unstudied deep-sea areas such as the Malta Trough.
areas dominated by gorgonians and living cold-water cor- The ROV surveys revealed new areas with extensive and
als with a rich variety of associated fauna. Black coral diverse CWC assemblages at depths of 300–1000 m extend-
(Leiopathes glaberrima) forests were dominant at 200– ing some 20 km along the edge of the Malta Graben. The
400 m, whilst stony reef-forming corals (in particular most abundant habitat-forming species on escarpments
Madrepora oculata) were most abundant in waters deeper included the scleractinian Madrepora oculata, the antipath-
than 500 m. The gorgonian Callogorgia verticillata was arian Leiopathes glaberrima and the alcyonacean Callogorgia
dominant in places over the entire depth range, but was verticillata (Figs. 22.1b and 22.2a). Several other locally
particularly abundant at depths of 800–1000 m. Such abundant habitat-forming species were also encountered,
cold-water coral assemblages are of high conservation including Acanthogorgia hirsuta, Corallium rubrum,
interest, and offshore marine protected areas are urgently Dendrobrachia bonsai, Lophelia pertusa, Muriceides lepida,
required in order to protect these very diverse, but highly Paramuricea macrospina, Placogorgia massiliensis, Swiftia
vulnerable, deep-sea habitats. pallida and Villogorgia bebrycoides (Fig. 22.2b). Colonies
of the precious red coral C. rubrum were observed at depths
Keywords of down to 1016 m, which represents the first time that this
Alcyonacea · Anthozoa · Antipatharia · Biodiversity · species has been recorded at depths exceeding 800 m
Central Mediterranean · Scleractinia · Sicily channel (Knittweis et al. 2016). A high diversity of associated fauna
(especially sponges, echinoderms, molluscs, crustaceans and
fish) was also present.
Malta hosts one of the six cold-water coral (CWC) provinces The depth distribution of the corals and alcyonaceans
known from the Mediterranean, the ‘South Malta CWC revealed a vertical stratification in the presence of the main
province’ (Taviani et al. 2017; see also Chimienti et al., this habitat-forming taxa. L. glaberrima was the dominant spe-
volume). Observations of the deep sea surrounding the cies at depths of 200–400 m, where it formed black coral
Maltese Islands are scant and, with few exceptions (Freiwald forests, while the framework-forming M. oculata dominated
et al. 2009; Costantini et al. 2010), are mainly based on trawl in deeper waters, with peak abundances at depths of
surveys of sedimentary bottoms. In June–July 2015, remotely 500–700 m. Alcyonaceans had a more patchy distribution
operated vehicle (ROV) surveys in Maltese waters were car- but C. verticillata was dominant in places, particularly at
ried out by the research vessel ‘Oceana Ranger’ as part of depths of 800–1000 m.
the project ‘LIFE BaĦAR for N2K’ (“Benthic Habitat These recent findings indicate that the deep sea around
Research for Marine Natura 2000 Site Designation”; see Malta represents an important biodiversity hotspot with a
variety of different assemblages dominated by sessile suspen-
L. Knittweis · J. Evans · J. A. Borg · P. J. Schembri (*) sion feeders (mainly cnidarians) as habitat-forming taxa. The
Department of Biology, University of Malta, Msida, Malta Malta Trough, in particular, seems to serve as a conduit for
Levantine Intermediate Water (LIW) (Freiwald et al. 2009;
R. Aguilar · H. Álvarez · S. García Chimienti et al., this volume; Hayes et al., this volume), trans-
Fundación Oceana, Madrid, Spain

https://doi.org/10.1007/978-3-319-91608-8_22
254 L. Knittweis et al.
Fig. 22.1 (a) Map of the Maltese Islands showing the sites with living blue shading) are also shown. (b) Relative abundance (as percent of
cold-water corals (orange circles), identified during the 2015 survey. total sightings) of the three main habitat-forming species, Callogorgia
The partial extent of the 25-nautical mile Fisheries Management Zone verticillata (n = 312), Madrepora oculata (n = 387) and Leiopathes
(dark blue oval around the Maltese Islands), and the location of current glaberrima (n = 252), recorded from different depth intervals
Marine Protected Areas for benthic habitats in Maltese waters (light
Fig. 22.2 (a) Coral and alcyonacean assemblages formed by cies: Corallium rubrum (left), Dendrobrachia bonsai (centre), and
Madrepora oculata (left), Leiopathes glaberrima (centre), and Paramuricea macrospina (right). (Photo copyright: OCEANA © LIFE
Callogorgia verticillata (right), found at depths of 300–1000 m in BaĦAR for N2K)
Maltese waters. (b) Examples of locally abundant habitat-forming spe-
porting seston and thus providing favourable conditions for of marine habitat types for the selection of sites to be included
suspension feeders, which in turn provide habitats to a large in the national inventories of natural sites of conservation
diversity of associated fauna. Similarly, newly discovered interest” (UNEP/MAP/RAC-SPA 2006). Moreover, several
CWC grounds off Sardinia were found to occur at depths cor- of the identified species (C. rubrum, L. pertusa, L. glaber-
responding to the core of the LIW (Taviani et al. 2017). rima, M. occulata) are designated as ‘endangered’ in the
Cold-water coral reefs are included in Annex I of the EU IUCN Red List of anthozoans in the Mediterranean (IUCN
‘Habitats Directive’ (Natural habitat types of Community 2016). The present results thus highlight the need for the rel-
interest whose conservation requires the designation of spe- evant authorities to consider establishment of offshore
cial areas of conservation; Council Directive 92/43/EEC), marine protected areas in order to protect these very diverse,
and are listed in the UNEP/MAP/RAC-SPA “Reference list but highly vulnerable, deep-sea habitats.
22 Discoveries of Cold-Water Coral Assemblages in Maltese Waters 255
Acknowledgements The LIFE BaĦAR for N2K Project is 50% co- downloads/anzothoa_fact_sheet_final_baja.pdf. Accessed 5 Jan
financed by the EU LIFE+ Funding Programme (agreement number: 2017
LIFE12 NAT/MT/000845) and implemented by Malta’s Environment Knittweis L, Aguilar R, Alvarez H, et al (2016) New depth record of the
and Resources Authority (ERA), the University of Malta, Fundacion precious red coral Corallium rubrum for the Mediterranean. Rapp
Oceana, the Ministry for Sustainable Development, the Environment Comm Int Mer Médit 41:467
and Climate Change (MSDEC), and the Department for Fisheries and Taviani M, Angeletti L, Canese S, et al (2017) The “Sardinian cold-
Aquaculture within MSDEC. We thank the ERA – Environment water coral province” in the context of the Mediterranean coral
Protection Directorate and the Ministry for Transport and Infrastructure – ecosystems. Deep-Sea Res Part 2 Top Stud Oceanogr 145:61–78.
Continental Shelf Department for granting permits to undertake this https://doi.org/10.1016/j.dsr2.2015.12.008
work. UNEP-MAP-RAC/SPA (2006) Reference list of marine habitat types
for the selection of sites to be included in the national inventories of
natural sites of conservation interest. Available via RAC/SPA. http://
www.rac-spa.org/sites/default/files/doc_fsd/lrhm_en.pdf. Accessed
References 5 Jan 2017
Costantini F, Taviani M, Remia A, et al (2010) Deep-water Corallium

rubrum (L., 1758) from the Mediterranean Sea: preliminary genetic
characterisation. Mar Ecol 31:261–269
Council Directive 92/43/EEC of 21 May 1992 on the conservation of Cross References
natural habitats and of wild fauna and flora. OJ L 206, 22.7.1992.
https://eur-lex.europa.eu/eli/dir/1992/43/oj Chimienti G, Bo M, Taviani M, et al (this volume) Occurrence and bio-
Freiwald A, Beuck L, Rüggeberg A, et al (2009) The white coral com- geography of Mediterranean cold-water corals
munity in the Central Mediterranean Sea revealed by ROV surveys. Hayes D, Schroeder K, Poulain, PM, et al (this volume) Review of the
Oceanography 22:58–74 circulation and characteristics of intermediate water masses of the
IUCN (2016) The IUCN Red List of anthozoans in the Mediterranean. Mediterranean – implications for cold-water coral habitats
Available via IUCN. https://www.iucn.org/sites/dev/files/import/
Drop Chapter
Corals of Aphrodite: Dendrophyllia 23
ramea Populations of Cyprus
Covadonga Orejas, Carlos Jiménez, Andrea Gori,

Jesús Rivera, Claudio Lo Iacono, Didier Aurelle,
Louis Hadjioannou, Antonis Petrou,
and Katerina Achilleos
Abstract urge local authorities into enforcing protection/conserva-

The deep-sea of the Levantine Mediterranean basin is tion measures.
still a fairly undiscovered world. The outer insular shelf
of Cyprus, a gateway to the deep realm, is not an excep-
tion, as very few deep areas in the waters surrounding Keywords
this island have been explored up to now. Here we pres- Cold-water corals · Deep-water scleractinians ·
ent a brief overview of the discovery of an extraordinary Conservation · Levantine Mediterranean
population of the scleractinian Dendrophyllia ramea at
depths, substrate and densities which were previously
unknown for this species. Our efforts in better defining The deep-sea realm of the island of Cyprus is still a world to
the habitat of this unique and fragile coral population, be discovered. Aside from oil industry geological surveys,
along with solid evidence of alarming destruction the scarce scientific information available until the last years
(albeit unintentional) from fishing activity, will hopefully was only focused on the Eratosthenes Seamount (Galil and
Zibrowius 1998; Bell et al. 2011; Mayer et al. 2011;
C. Orejas (*) Wachsmann et al. 2011; Bell and Brennan 2013; Cornwell
Instituto Español de Oceanografía (IEO), Centro Oceanográfico de et al. 2013; Mitchell et al. 2013; unpublished cruise report
Baleares, Palma de Mallorca, Spain from Research Vessel (RV) Merian 2011). The morphologi-
cal and biological complexity of the regions around the
C. Jiménez Cyprus insular margin, from the continental shelf down to
Enalia Physis Environmental Research Centre (ENALIA),
the bathyal and abyssal sectors has not been explored until
Nicosia, Cyprus
now, and consequently it is largely unknown. The scarce
Energy, Environment and Water Research Centre (EEWRC)
information from these areas comes frequently from the
of The Cyprus Institute, Nicosia, Cyprus
local fishermen who are highly experienced in the area.
A. Gori
As part of the research project CYCLAMEN (TOTAL
Institut de Ciències del Mar, Consejo Superior de Investigaciones
Científicas, Barcelona, Spain foundation), in 2015 we conducted a research cruise on
board the RV Aegaeo (HCRM – Greece) in Cypriot waters
J. Rivera
Instituto Español de Oceanografía (IEO), Madrid, Spain off Protaras (South-eastern coast), with the aim of exploring
for the first time the outer shelf- upper slope region, between
C. Lo Iacono
National Oceanography Centre, University of Southampton 150 and 400 m depth, focusing on the cold-water coral
Waterfront Campus, Southampton, UK (CWC) communities. Previous information on the presence
D. Aurelle of corals in the area was reported by local fishermen who
Aix Marseille Univ, Avignon Université, CNRS, IRD, IMBE, found splendid specimens of Dendrophyllia colonies
Marseille, France (Fig. 23.1a). Before this cruise, it was thought that the main
Aix Marseille Univ, Université de Toulon, CNRS, IRD, MIO, species inhabiting the area was Dendrophyllia cornigera as
Marseille, France the skeletons from corals provided by fishermen represented
L. Hadjioannou · A. Petrou · K. Achilleos the only evidence available. However, after our exploration
Enalia Physis Environmental Research Centre (ENALIA), and sample collection with the remotely operated vehicle
Nicosia, Cyprus

https://doi.org/10.1007/978-3-319-91608-8_23
258 C. Orejas et al.
Fig. 23.1 (a) Skeleton of a

Dendrophyllia sp. specimen
collected by a local fisherman,
(b) large colony of D. ramea
off Protaras at ca. 145 m
depth. Distance between the
laser pointers is 10 cm, (c)
colony of D. ramea lying on
the sandy substrate. White
arrows point out to two
polyps growing away from
the sediment. (Photographs:
a: © Carlos Jiménez; b and c:
© CYCLAMEN project (With
permission from JCRS:
Galaxea J. Coral Reef Stud.
19: 15–16, Orejas et al. 2017
Fig. 1b))
(ROV) MAXROV and subsequent preliminary molecular from negligible in the study site. Strong surges related to sea-
analysis (mitochondrial COI and nuclear histone H3), there sonal storms able to destroy and fragment the largest colo-
was evidence indicating that the Dendrophyllidae inhabiting nies, are not expected to affect the Dendrophyllia population,
the soft bottoms off Protaras was a rather slender form of D. being deeper than the maximal depth of wave action known
ramea (Fig. 23.1b, Orejas et al. 2017). These findings were in the Mediterranean Sea. However, strong bottom currents
quite unexpected since D. ramea is described inhabiting could presumably affect locally the stability of small colo-
hard-substrates normally shallower than 100 m depth (e.g. nies. The most plausible explanation for the high frequency
Zibrowius 1980; Brito and Ocaña 2004; Salvati et al. 2004; of upturned colonies observed is the impact of fishing activi-
Orejas et al. 2017 and references therein; see Altuna and ties (recreational and, on a lesser extent, commercial).
Poliseno, this volume; Chimienti et al., this volume). An iso- Fishing pressure (e.g. bottom nets) is significant in the area
lated D. ramea colony in the Ionian Sea was found estab- of the Dendrophyllia population (Orejas et al. 2017); the his-
lished on a shallow sedimentary slope; however, the coral tory of this activity is being currently under revision (Jiménez
most probably was attached to the underlying hard-substrate et al. work in progress).
(Salomidi et al. 2010). At a first glance, the Dendrophyllia population seemed to
The D. ramea colonies found in the area off Protaras dis- be poor in terms of associated species. However, after a
played a variety of growth forms with some specimens of closer inspection of the coral specimens collected during the
very large dimensions (~40 to 50 cm length; Fig. 23.1b). cruise, an abundant associated fauna was found, with 48 spe-
Interestingly, some live colonies were over the seafloor with cies being identified as epibionts on the corals (Fig. 23.2,
the basal portions conspicuously turned up or exposed. These Jiménez et al. 2016a). Bryozoans and serpulid polychaetes
colonies displayed a singular polyp growth orientation in were most represented on the dead portions of the coral
which the tips appear to re-direct the growth axis away from colonies.
the sedimentary bottom (Fig. 23.1c). This orientated growth Beside the coral population, other biocoenoses have been
could be a response to periodic disturbances that cause observed in the surveyed areas: (1) bottoms dominated by
upturning of entire colonies and possibly fragmentation. Cidaridae sea urchins (115–240 m depth), (2) bottoms
Abundant small-sized (~5 to 10 cm length) branches scat- dominated by Cerianthus sp. (105–175 m depth), (3) bot-
tered on the bottom suggest physical disturbances are far toms dominated by Alcyonium palmatum (120–145 m depth)
23 Corals of Aphrodite: Dendrophyllia ramea of Cyprus 259
Fig. 23.2 Examples of the

biodiversity found associated
to the specimens of
Dendrophyllia ramea
collected off Protaras; (a)
specimen of the solitary coral
Caryophyllia calveri, (b)
specimens of the polychaetes
Placostegus tridentatus (red
arrows) and Janita frimbiata
(blue arrow) and the
bryozoans Escharina vulgaris
(black arrow), (c) specimens
of the bryozoans Puellina
hincksi; scale bar = 100 μm
and (d) specimens of the
bryozoan Puellina
pedunculata; scale bar =
100 μm. (Photographs: ©
C. Jiménez and K. Achilleos)
and (4) bottoms dominated by pennatulaceans (~130 m “Vulnerable”. Recently the species has also been included in
depth). These first explorations point out a relatively rich and the Annex II of Barcelona Convention. Currently, the results
diverse megabenthic fauna in this area of the Levantine of our study, together with other initiatives (e.g.
Mediterranean basin, which remains unexplored in most PROTOMEDEA project to suggest management areas in
parts, and where more research efforts are needed especially Greece and Cyprus) are forming the basis for proposing to
in the deep benthic realm. Studies on deep-sea benthic habi- the local authorities the protection of the area around the
tats will contribute to enlarge the knowledge on the biodiver- Dendrophyllia populations.
sity of the Levantine deep-sea realm contributing also to
detect the potential occurrence of non –indigenous invasive Acknowledgements This chapter is dedicated to the memory of Félix
species, a threat that has been documented since years in Descalzo Gómez a great fellow of many unforgettable research cruises
and a close and dear friend. We are grateful to Marzia Bo and Jordi
shallow waters for the eastern Mediterranean and completely Grinyó for their comments which help to improve the quality of the
unstudied in deep-sea areas (see Galil, this volume). As manuscript. Thanks are due to the scientific team of CYCLAMEN, the
recently as 2017, on two independent events, fishermen from crew and HCMR-ROV team of the RV Aegaeo, and the Department of
Protaras utilising bottom nets inside the area with corals Fisheries and Marine Research in Cyprus. This work has been con-
ducted within the CYCLAMEN project funded by the TOTAL founda-
caught in their nets (aside from Dendrophyllia colonies) a tion (BIO_2014_091_Juin_CS-8).
juvenile and a young adult of the invasive lionfish (Pterois
miles), which is spreading around Cyprus and the Levantine
Sea in general (Jimenez et al. 2016b and work in progress).
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Cold-Water Corals in Fluid Venting 24
Submarine Structures
Desirée Palomino, José Luis Rueda, Juan Tomás Vázquez,

Javier Urra, Olga Sánchez-Guillamón, Emilio González-
García, Nieves López-González,
and Luis Miguel Fernández-Salas
Abstract Both colonial and solitary scleractinian cold-water corals

A relationship between scleractinian cold-water corals (CWCs), as well as other sessile cnidarians (e.g. antipathar-
and fluid venting submarine structures has been observed ians, octocorals, etc.), have been widely documented from
in Mediterranean and adjacent areas. Mud volcanoes and fluid venting submarine structures (FVSS) of the
mud diapirs promote different substrate types for biologi- Mediterranean Sea (e.g. western Alborán Sea, southeastern
cal colonisation: from muddy bottoms with Adriatic Sea) (Margreth et al. 2011; Somoza et al. 2012;
chemosynthesis-based communities and typical bathyal Angeletti et al. 2015; Rüggeberg and Foubert, this volume;
soft bottom fauna to hard bottoms with sessile solitary Wienberg, this volume) and adjacent areas exposed to
and colonial scleractinian cold-water corals, sponges, Mediterranean water masses (e.g. Gulf of Cádiz) (Wienberg
octocorals and antipatharians. Fluid venting submarine et al. 2009; León et al. 2012; Palomino et al. 2016; Rueda
structures provide an elevated position for the develop- et al. 2016). During the last decades, FVSS mainly driven by
ment of sessile suspension feeders, including scleractin- tectonic processes have been detected in bathyal areas with
ian cold-water corals, where an interaction of the currents compressive (e.g. Gulf of Cádiz, Mediterranean Ridge,
with the local topography generally accelerates the water Western Alborán Sea) and extensional (e.g. Black Sea,
flow. This facilitates the supply of suspended food parti- Tyrrhenian Sea) settings. The uplift of massive plastic sedi-
cles and the development of carbonate mounds mainly mentary rocks as mud diapirs (MDs) and the vertical migra-
built by scleractinian cold-water corals. Methane-derived tion and extrusion of fluids (hydrocarbon, brines, etc.) and
authigenic carbonates provide hard substrates, which rep- muddy sediments as mud volcanoes (MVs) promote differ-
resent a prerequisite for larvae settlement of some sclerac- ent substrate types for biological colonisation. Particularly,
tinian cold-water corals and further development of muddy bottoms composed of gas-rich mud breccias may be
polyps and colonies in those elevated areas. These factors later replaced by hard bottoms of methane-derived authi-
make FVSS an appropriate place for the development of genic carbonates (MDACs) (slabs, chimneys, crusts, etc.),
habitats conformed by scleractinian cold-water corals as according to the development stages of the MVs and MDs
well as genuine and singular biodiversity hotspots. proposed by León et al. (2007), which was later adapted by
Palomino et al. (2016) to different seepage and bottom cur-
Keywords rent scenarios. This model proposes a biological differentia-
Cold-water coral · Seepage · Authigenic carbonates · tion from chemosynthesis-based communities with typical
Habitat · Mediterranean Sea bathyal soft-bottom fauna (e.g. sea pens) in anoxic mud
breccia bottoms where fluid venting occurs, to communities
dominated by hard bottom sessile solitary and colonial sus-
D. Palomino (*) · J. L. Rueda · J. T. Vázquez · J. Urra
pension feeders such as scleractinian CWCs, sponges, octo-
O. Sánchez-Guillamón · N. López-González
Centro Oceanográfico de Málaga, Instituto Español de corals (gorgonians and soft corals) and antipatharians. The
Oceanografía, Fuengirola, Spain development of MVs through time, according to this model,
e-mail: [email protected] generally starts with an active fluid flow and mud extrusion
E. González-García that build up the volcanic edifice where benthic communities
Facultad de Ciencias, Universidad de Málaga, Málaga, Spain associated with seepage (mainly chemosynthetic bacteria as
L. M. Fernández-Salas well as chemosymbiotic bivalves and polychaetes) are
Centro Oceanográfico de Cádiz, Instituto Español de Oceanografía, favoured (Fig. 24.1a). This first stage is followed by m
oderate
Cádiz, Spain

https://doi.org/10.1007/978-3-319-91608-8_24
262 D. Palomino et al.
Fig. 24.1 Development of mud volcanoes through time: (a) active pens), and (c) MDACs exhumed in some areas and colonised by scler-
fluid flow and mud extrusion with the establishment of chemosymbiotic actinian CWCs and other sessile suspension feeders (e.g. sponges,
fauna, (b) moderate to low seepage and formation of MDACs as well as antipatharians, octocorals). (Modified from Palomino et al. 2016)
the colonisation of soft bottoms by typical soft bottom fauna (e.g. sea
to low seepage that promotes the formation of MDACs by growth. Nevertheless, when sedimentation rates are higher
methane anaerobic oxidation by different archeobacteria. than scleractinian CWC growth rates or when a new migra-
Contourite deposits can occur on MVs and MDs flanks as tion and extrusion of muddy sediments occurs in FVSS,
result of a higher bottom current velocity. These deposits are deposits can lead to the burial and ultimate demise of the
generally colonised by soft bottom epifauna such as sea habitats conformed by all these sessile organisms (León
pens (e.g. Kophobelemnon, Funiculina), crinoids (e.g. et al. 2007; Wienberg et al. 2010; Margreth et al. 2011;
Leptometra), solitary scleractinians (e.g. Flabellum) and Mienis et al. 2012). The MDACs are formed inside sedi-
both desmosponges (e.g. Thenea) and hexactinellid sponges ments of MVs and MDs, and exhumed where bottom cur-
(e.g. Pheronema, Hyalonema) (Fig. 24.1b). Finally, the rents are strong enough to remobilise unconsolidated
development is characterised by latent conditions where the surficial sediments (Magalhães et al. 2012). These MDACs
MDACs are exhumed by bottom current action and colo- increase the seafloor habitat complexity by providing differ-
nised by hard bottom sessile suspension feeders (e.g. scler- ent types of hard substrates (e.g. crusts, chimneys, slabs),
actinian CWCs) which further increase the bottom which represents a prerequisite for larvae settlement of
complexity, the biological productivity and the biodiversity. some scleractinian CWCs and further development of pol-
In this stage, bottom currents should be strong enough for yps and colonies in those elevated areas that have an ade-
promoting a continuous availability of food particles for the quate food supply (Angeletti et al. 2015; Rueda et al. 2016).
scleractinian CWCs and other sessile suspension feeders Hovland et al. (1998) proposed the “Hydraulic theory” that
such as the octocorals and the antipatharians (Fig. 24.1c). links scleractinian CWC growth to seepage in FVSS,
Unlike other types of FVSS (e.g. pockmarks), MVs and because fluid flow may provide an extra local input of nutri-
MDs provide an elevated position for the development of ents throughout the seabed where scleractinian CWCs
scleractinian CWCs and other sessile suspension feeders develop. In addition, bacterial productivity (heterotrophic
(e.g. antipatharians, sponges, sea pens) with respect to adja- and chemosynthetic) seems to increase in FVSS when com-
cent bottoms. As observed in other elevated seafloor struc- pared to adjacent soft bottoms without seepage, and this has
tures (e.g. ridges, seamounts), scleractinian CWCs and been hypothesised to act as extra nutrient sources for higher
other suspension feeders of MVs and MDs could be bene- trophic organisms such as scleractinian CWCs. Nevertheless,
fited from the interaction of the currents with the local this theory is under debate and no clear evidence has been
topography, which accelerates the water flow (Genin et al. found yet on the relationship between those habitat-forming
1986). Strong bottom currents also facilitate the supply of organisms and seepage.
suspended food particles and the development of carbonate In the Montenegrin margin (southeastern Adriatic Sea),
mounds mainly built by scleractinian CWCs and of other a spectacular field of exhumed and vertically-placed chim-
vulnerable marine ecosystems (VMEs) (e.g. sponge fields) neys related to hydrocarbon venting serves as substrate for
in these FVSS (Freiwald and Roberts 2005). Suspended a wide variety of sessile megafauna, including scleractin-
sediments can also be trapped and baffled into the coral ian CWCs (e.g. Madrepora oculata, Dendrophyllia corni-
framework, contributing to coral mound stabilisation and gera, Caryophyllia sp.), large octocorals (e.g. Callogorgia
24 Cold-Water Corals in Fluid Venting Submarine Structures 263
verticillata), antipatharians (e.g. Leiopathes) and desmo- Freiwald A, Roberts JM (2005) Cold-water corals and ecosystems.
Springer, Heidelberg, p 1243
sponges (e.g. Pachastrella) (Angeletti et al. 2015). In the Genin A, Dayton PK, Lonsdale PF, et al (1986) Corals on seamount
Gulf of Cádiz, scleractinian CWCs (e.g. M. oculata, peaks provide evidence of current acceleration over deep-sea topog-
Lophelia pertusa and D. cornigera) as well as antipathari- raphy. Nature 322:59–61
ans (Anthipathella, Leiopathes) and large sponges (e.g. Hovland M, Mortensen PB, Brattegard T, et al (1998) Ahermatypic
coral banks off mid-Norway: evidence for a link with seepage of
Petrosia sp., Asconema setubalense) colonise MDACs of light hydrocarbons. PALAIOS 13:189–200
some FVSS (e.g. Gazul MV) (Palomino et al. 2016; Rueda León R, Somoza L, Medialdea T, et al (2007) Sea-floor features related
et al. 2016). The presence of scleractinian CWCs in these to hydrocarbon seeps in deepwater carbonate mud mounds of the
FVSS also promotes the occurrence of typical associated Gulf of Cádiz: from mud flows to carbonate precipitates. Geo-Mar
Lett 27:237–247
species such as the polychaete Eunice norvegica and the León R, Somoza L, Medialdea T, et al (2012) New discoveries of
gastropod Hirtomurex (=Coralliophila) squamosa (Rueda mud volcanoes on the Moroccan Atlantic continental margin
et al. 2016, this volume). FVSS with CWCs are very sensi- (Gulf of Cadiz): morpho-structural characterization. Geo-Mar Lett
tive to some human activities impacting the seabed such as 32:473–488
Magalhães VH, Pinheiro LM, Ivanov MK, et al (2012) Formation pro-
mining and trawling (see Otero and Marin, this volume), cesses of methane-derived authigenic carbonates from the Gulf of
and policy measures of conservation must be taken in Cadiz. Sediment Geol 243–244:155–168
order to protect the singular occurrence of a combination Margreth S, Gennari G, Rüggeberg A, et al (2011) Growth and demise
of two different habitats included in the EU Habitat of cold-water coral ecosystems on mud volcanoes in the West
Alboran Sea: the messages from planktonic and benthic foramin-
Directive (92/43/EEC) such as the Reefs (Habitat 1170) ifera. Mar Geol 282:26–39
and the Submarine structures made by leaking gases Mienis F, De Stigter HC, De Haas H, et al (2012) Hydrodynamic condi-
(Habitat 1180). Nevertheless, CWCs are sometimes tions in a cold-water coral mound area on the Renard Ridge, south-
located in low trawling activity areas because of the pres- ern Gulf of Cadiz. J Mar Syst 96–97:61–71
Palomino D, López-González N, Vázquez JT, et al (2016)
ence of hard bottoms and strong bottom currents, which Multidisciplinary study of mud volcanoes and diapirs and their rela-
altogether result in higher abundances and biomasses of tionship to seepages and bottom currents in the Gulf of Cádiz conti-
benthic organisms (Rueda et al. 2016, this volume). nental slope (northeastern sector). Mar Geol 378:196–212
Although there are still some knowledge gaps on the rela- Rueda JL, González-García E, Krutzky C, et al (2016) From
chemosynthesis- based communities to cold-water corals: new
tionship between CWCs and FVSS, the case study in the records of vulnerable deep-sea habitats for the Gulf of Cádiz. Mar
Mediterranean and adjacent areas suggests that the combina- Biodivers 46:473–482
tion of: (a) the stable hard substrate provided by MDACs for Somoza L, Medialdea T, León R, et al (2012) Structure of mud
larval settlement and colonial development; (b) the elevated volcano systems and pockmarks in the region of the Ceuta
Contourite Depositional System (Western Alborán Sea). Mar Geol
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ticles, makes some FVSS a suitable place for the develop- corals in the Gulf of Cádiz-first clues about their spatial and temporal
ment of habitats conformed by scleractinian CWCs as well distribution. Deep-Sea Res Part 1 Oceanogr Res Pap 56:1873–1893
Wienberg C, Frank N, Mertens KN, et al (2010) Glacial cold-water
as genuine and singular biodiversity hotspots. coral growth in the Gulf of Cádiz: implications of increased palaeo-
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Acknowledgements This work has been developed as part of the
LIFE+ INDEMARES/CHICA (LIFE07/NAT/E/000732) and
SUBVENT (CGL2012-39524-C02-01) projects. We thank the two
reviewers Dr. Claudia Wienberg and Dr. Gemma Ercilla for construc-
tive comments that served to improve the manuscript. Cross References
References ciated fauna in the Mediterranean Sea and adjacent areas
Rüeggeberg A, Foubert A (this volume) Cold-water corals and mud vol-
Angeletti L, Canese S, Franchi F, et al (2015) The “chimney forest” of canoes: life on a dynamic substrate
the deep Montenegrin margin, southeastern Adriatic Sea. Mar Pet Wienberg C (this volume) A deglacial cold-water coral boom in the
Geol 66:542–554 Alborán Sea: from coral mounds and species dominance
Drop Chapter
Cold-Water Corals and Mud Volcanoes: 25
Life on a Dynamic Substrate
Andres Rüggeberg and Anneleen Foubert
Abstract escarpments and ridges (Foubert et al. 2008; Knittweiss

Mud volcanoes are prominent features in distinct areas of et al., this volume), on knolls and banks (De Mol et al. 2012;
the Mediterranean Sea and the Gulf of Cádiz. Cold-water Lo Iacono et al., this volume) and mounds (Taviani et al.
corals use these elevated structures as substrate and 2005; Comas and Pinheiro 2007; Lo Iacono et al., this vol-
develop coral reefs during periods of suitable environ- ume), at cliffs and canyons (e.g., Freiwald et al. 2009; Orejas
mental conditions. So far, this partnership has only been et al. 2009; Fabri et al. 2014; Angeletti et al., this volume;
reported from the Alborán Sea and the Gulf of Cádiz, Aymà et al., this volume; Fourt et al., this volume; Lastras
where they occurred during the Bølling-Allerød to early et al., this volume; Puig and Gili, this volume) and on mud
Holocene and during the mid to late Holocene. volcanoes (e.g., Wienberg et al. 2009; Margreth et al. 2011;
Palomino et al., this volume). Gardner (2001) was one of the
Keywords first to report CWC debris overlying mud breccia on an inac-
Cold-water corals · Mud volcanoes · Substrate tive mud volcano from the Gulf of Cádiz offshore Morocco.
availability · Environmental control The temporal and spatial distribution of reef-building CWCs
in the Mediterranean Sea and the Gulf of Cádiz has been
related to areas with high surface productivity and vigorous
Reef-building cold-water corals (CWC) like Lophelia per- intermediate water mass circulation (Wienberg et al. 2010;
tusa and Madrepora oculata are prominent features within Fink et al. 2015), however, these bioherms also need a nucle-
the Mediterranean Sea and the Gulf of Cádiz (e.g., Freiwald ation point, a substratum.
et al. 2009; Wienberg et al. 2009; Altuna and Poliseno, this Mud volcanoes are one possible niche for CWCs to
volume; Chimienti et al., this volume; Rueda et al., this vol- inhabit. In the Mediterranean Sea and the Gulf of Cádiz (see
ume). However, most of the reported occurrences refer to Palomino et al., this volume) they have been frequently
fossil remnants while living occurrences are less abundant reported in areas evidencing a dynamic sub-seafloor with
and exhibit a rather scattered distribution pattern compared active seepage of fluids and hydrocarbons (Fig. 25.1a). In the
to those known from the North Atlantic (Fig. 25.1a; Fink Gulf of Cádiz mud volcanoes are clustered in distinct fluid
et al. 2015; see Taviani et al., this volume; Vertino et al., this venting provinces like the Spanish-Moroccan and El Arraiche
volume). Flögel et al. (2014) described the CWC appearance fields along the Moroccan margin (Gardner 2001; Van
in these areas from patchy growth forms with small colonies Rensbergen et al. 2005) or the Guadalquivir diapiric ridge
including larger patches of fine-grained sediments or coral and Tasyo fields along the Spanish margin (Somoza et al.
rubble to only small and frequently isolated branches/colo- 2003). In the eastern Mediterranean, mud volcanoes were
nies or even single living polyps. The main habitat of the first discovered west of Crete on the Mediterranean Ridge
coral reefs in the Mediterranean Sea is at intermediate depths (Cita et al. 1981). Intensive investigation followed with the
between 250 and 650 m (Freiwald et al. 2009; see Chimienti discovery of numerous new mud volcanoes (Limonov et al.
et al., this volume) but also deeper for the mainly fossil cor- 1996) being active since 1 Ma on the northern margin of the
als in the Gulf of Cádiz. These corals have been described on Mediterranean Ridge (Robertson and Ocean Drilling
Program Leg 160 Scientific Party 1998) and even longer
A. Rüggeberg (*) · A. Foubert since 3 Ma along the Calabrian Arc (Praeg et al. 2009).
Department of Geosciences, University of Fribourg, Occurrence of mud volcanism and diapirism in the eastern
Fribourg, Switzerland Mediterranean is also recorded in an extensional setting of

https://doi.org/10.1007/978-3-319-91608-8_25
266 A. Rüggeberg and A. Foubert
Fig. 25.1 (a) Overview map of the Mediterranean Sea showing the Espejo et al. 2008) and during the later Holocene [coral dates from
mud volcano provinces, the reefal cold-water coral areas and the McCulloch et al. (2010), Margreth et al. (2011), Fink et al. (2013), and
general ocean circulation pattern in the Mediterranean Sea (Modified Stalder et al. (2015)]. Potential drivers controlling coral development
from Fink et al. 2015 and references therein). Black arrows correspond are productivity [reconstructions from Rodrigo-Gámiz et al. (2011,
to surface water circulation, dotted black arrows to the intermediate solid black) and Fink et al. (2013, dotted grey)], water mass properties
water circulation, respectively. Indicated are the sampling sites of fossil [temperature: Deep Water Temperature (DWT, dotted grey) from Cacho
corals (circles) and living occurrences (stars) solely considering the two et al. (2006), Sea Surface Temperature (SST, solid black) from Cacho
framework-forming species Lophelia pertusa and Madrepora oculata et al. (2001); Salinity reconstructions from Emeis et al. (2000, solid
(From Fink et al. 2015). Co-occurrence of mud volcanoes and cold- black) and Cacho et al. (2006, dotted grey)], which are influenced by
water corals has been reported for the GoC and the WAB. Map by regional climatic conditions [reconstructions from Adkins et al. (2006,
Ocean Data View (Schlitzer 2016). (b) Idealised schematic of a mud solid black) and Fink et al. (2013, dotted grey)]. African humid period
volcano and a core log from a gravity corer (GC) with alternating occurred between 14.8 and 5.5 ka (deMenocal et al. 2000). MAW
sediments of episodic mud flows, coral settlement on mud breccia and Modified Atlantic Water, WIW Winter Intermediate Water, LIW
later burial phases (modified after Spezzaferri et al. 2015 and Margreth Levantine Intermediate Water, LGM Last Glacial Maximum, OD Older
et al. 2011). For the settlement of reef-building corals habitable Dryas, B/A Bølling-Allerød, YD Younger Dryas, S1 Sapropel layer 1.
conditions within the right nutrient window and a well-defined Light green layers indicate CWC occurrences at Maya and Dhaka mud
hydrodynamic regime are required. In the Alborán Sea, these conditions volcanoes, dark green layers highlight occurrences of dated corals from
occurred during Organic Rich Layer 1 (ORL1) (14.5–8.2 ka, Jimenez- the Alborán Sea
the Nile Deep Sea Fan (Dupré et al. 2007). In the western seepage-related structures on both the Spanish and the
Mediterranean, mud volcanoes are relative scarce features Moroccan margin of the West Alborán Basin (Gennari et al.
only reported from the Alborán Sea, where they are related to 2013). Mud volcanoes are dome-shaped formations on the
mud diapirs and active sediment and fluid flow in a back-arc seafloor of up to 10 km in diameter and 700 m in height,
basin setting (e.g., Comas et al. 2010). Several expeditions which are created by the release of mud charged with
revealed the existence of mud volcanoes, pockmarks and hydrocarbon-rich fluids derived from the sub-seafloor.
25 Cold-Water Corals and Mud Volcanoes: Life on a Dynamic Substrate 267
However, their common appearance in the Mediterranean Alborán Sea indicating that the coral reefs possibly lasted for
Sea is generally smaller being 100–200 m high and 1–5 km some hundreds to thousands of years (based on 14C age dates
across (Woodside et al. 2006). During their active phase, the of sediments) before environmental conditions (dissolved
build-up of pressure in wet and gassy sediments below faults oxygen, salinity and density, nutrient availability) changed
leads to periodical eruptions of mud and fluids with rock and they became buried by a hemipelagic sediment cover.
fragments, the so-called mud breccia (Cita et al. 1981), a Dated coral fragments (McCulloch et al. 2010; Fink et al.
semi-liquid, clayey matrix containing various amounts of 2013; Stalder et al. 2015) support the occurrence of reefs in
heterogenic rock fragments and clasts derived from the the Alborán Sea during Organic Rich Layer 1 (ORL 1, 14.5–
geological section through which the mud ascends (Cita 8.2 ka; Jimenez-Espejo et al. 2008) and the African humid
et al. 1981; Staffini et al. 1993; Dimitrov 2002; Kopf 2002). period (deMenocal et al. 2000; Castañeda et al. 2009) and
Successive episodes of mud flows as a result of degassing after sapropel layer 1 (<6 ky; Rohling 1994). Both episodes
processes in the deep sub-seafloor and the progressive are marked by pulses or periods of higher productivity or
accumulation of extruded mud breccia build up the cone- enhanced nutrient supply to the surface waters and a change
shaped edifice, forming the mud volcano (Fig. 25.1b). If not in climatic conditions – from dry to humid climates or vice
visually ground-truthed by remotely operated vehicles versa (Fig. 25.1b). Rising seawater temperatures and
(ROVs) or deep-towed camera, the identification of mud salinities occurred during ORL1 indicating a cooler episode
volcanoes through (gravity) coring is necessary to retrieve at the onset of coral growth. At a later stage ~10 ka the coral
sequences with greyish mud breccia sediment from targets reefs experienced a change in water masses to much higher
selected on the basis of multibeam bathymetry/backscatter temperatures in conjunction with the rising sea level. At that
or side-scan sonar (Fig. 25.1b). As most of the mud volcanoes time the African humid period intensified leading to a
are presently not active (e.g., Niemann et al. 2006), their decrease in productivity and possibly decreasing oxygen
surficial sediment consists mainly of hemipelagic contents in the bottom waters (Fink et al. 2015). The CWCs
foraminifera-rich sandy mud. of the Late Holocene profit from more stable oceanographic
It is the habitat complexity with clasts exhumed by the (T, S, O2) and drier climatic conditions. Their growth stopped
mud breccia and possible authigenic carbonates as remnants around 2 ka at Dhaka mud volcano; only a few records of
of cold-seep communities, which provide the basis for new CWC in the Alborán Sea are reported for the past 1.5 kyr
life – as hard substrate for a new community of CWCs and/ during times with high climatic variability and lower surface
or other species to grow and develop (see also Palomino productivity (Fig. 25.1b).
et al., this volume). The occurrence of hard substrata on mud The occurrence of CWC on mud volcanoes, which pro-
volcanoes allows the preferential settlement of sessile vide a (temporal) niche for a higher diverse benthic com-
organisms attached to the seafloor (León et al. 2007) – not munity compared to the adjacent soft bottoms (see Palomino
possible on the soft sediments of the surrounding seafloor. et al., this volume; see Rueda et al., this volume), is the
However, if substrate availability would be the only result of the complex interplay of environmental processes.
controlling factor, coral patches and reefs would be thriving The examples of the Alborán Sea are corroborated by the
on the summits and flanks of mud volcanoes – if not occurrences in the Gulf of Cádiz, evidencing that nutrition
temporarily disturbed by mud volcano activity. Besides and its distribution through currents at the interface of
substrate availability and the absence of destructive extrusive water masses are the most important processes. However,
events, other environmental factors control the distribution they can vary in strength pending on the prevailing and
of CWC growth in those vulnerable environments. dominating climatic factors. Therefore, the complexity of
Comparable to what has been suggested by Becker et al. the benthic ecosystems needs more continuous and inte-
(2009) for the Gulf of Mexico or León et al. (2012) and grated monitoring of the extrinsic controlling factors to bet-
Somoza et al. (2003) for the Gulf of Cádiz, mud breccia and ter understand their proliferation and limitation of growth
authigenic carbonate substrata together with the higher on temporal substrates available at the surface of mud
productivity and stronger hydrodynamic processes at the volcanoes.
interface between two water masses (surface or upper
intermediate with lower intermediate, Fig. 25.1b) drive the Acknowledgments This study has been developed as part of the SNF-
CWC communities at mud volcanoes in the western funded project 4D-Diagenesis@Mound (SNF project n° 200021–
149247). We are grateful to the editors and both reviewers Dr. Luis
Mediterranean and the Gulf of Cádiz (Fink et al. 2013; Pinheiro and Dr. Claudia Wienberg for very helpful and constructive
Stalder et al. 2015; Palomino et al., this volume). The comments to improve the manuscript. We dedicate this study to Jean-
nucleation of corals on mud breccia in the fossil record has Pierre Henriet (1945–2017) for his influence and visionary work
been described by Margreth et al. (2011) for the Maya steering interdisciplinary research on cold-water corals and mud
volcanoes.
(~15 ka) and Dhaka (~4 ka) mud volcanoes in the western
268 A. Rüggeberg and A. Foubert
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Occurrence of Living Cold-Water Corals
at Large Depths Within Submarine 26
Canyons of the Northwestern
Mediterranean Sea
Anna Aymà, Jacopo Aguzzi, Miquel Canals,

Joan Batista Company, Galderic Lastras, Ariadna Mecho,
and Claudio Lo Iacono
Abstract coral populations, locally extending to water depths

In the northwestern Mediterranean Sea, cold-water cor- below 1000 m.
als Madrepora oculata, Lophelia pertusa, Dendrophyllia
cornigera and Desmophyllum dianthus have been mostly
described at relatively shallow depths (i.e. <400 m). Keywords
Here, we report the results of the inspection of the large, Northwestern Mediterranean Sea · Submarine canyons ·
deeply incised Cap de Creus, La Fonera and Blanes sub- Cold-water corals (CWC) · Deep water · Remotely
marine canyons in order to assess the presence of cold- operated vehicle (ROV) · Agassiz trawl (AGT)
water corals at depths between 600 and 1500 m. Two
complementary methodologies were applied: remotely
operated vehicle dives for in situ observation, and
Agassiz trawls to get biological samples. Remotely 26.1 Introduction
operated vehicle videos pictured aggregations of speci-
mens of the solitary D. dianthus at 1409 m depth in La Deep-sea ecosystems constitute the largest biome on
Fonera Canyon, which seemed to be alive. This is the Earth. They cover more than 65% of the planet surface and
first in situ observation of this species at such depths in encompass more than 95% of the global biosphere
the northwestern Mediterranean Sea. Agassiz trawl sam- (Danovaro et al. 2010). The beginning of the exploration
ples provided living M. oculata and L. pertusa in Blanes of the deep Mediterranean Sea dates back to the end of the
Canyon at 1200 and 900 m depth, respectively. They eighteenth century (Ryland 2000), and the sampling effort
also yielded living D. dianthus in Cap de Creus Canyon has constantly increased since then. In the western
at 900 m and in Blanes Canyon at 900 and 1200 m depth. Mediterranean Sea several studies have been carried out,
Jointly with other recently published results, our find- mostly by trawling, in order to obtain comprehensive fau-
ings demonstrate that submarine canyons in the north- nal lists and define the geographic and bathymetric distri-
western Mediterranean Sea host significant cold-water bution ranges of species (Cartes and Sarda 1989; Bouchet
and Taviani 1992; Cartes et al. 1993, 2009; Abello et al.
2002; D’Onghia et al. 2004, this volume; Galil 2004; Sion
A. Aymà · M. Canals (*) · G. Lastras et al. 2004; Papiol et al. 2012; Aguzzi et al. 2013; Fanelli
GRC Geociències Marines, Departament de Dinàmica de la Terra i
et al. 2013; Tecchio et al. 2013; Mecho et al. 2014a, b;
de l’Oceà, Facultat de Ciències de la Terra, Universitat de
Barcelona, Barcelona, Spain Rueda et al., this volume).
e-mail: [email protected] The search for cold-water corals (CWCs) progressively
J. Aguzzi · J. B. Company · A. Mecho gained scientific and socioeconomic interest, especially in
Institut de Ciències del Mar (ICM-CSIC), Barcelona, Spain the last two decades (Roberts et al. 2006, 2009). Similarly to
Millennium Nucleus of Ecology and Sustainable Management of shallow-water tropical corals, deep-sea CWC reefs host high
Oceanic Islands (ESMOI), Universidad Católica del Norte, biodiversity (Henry and Roberts 2007; Mastrototaro et al.
Coquimbo, Chile 2010; Purser et al. 2013) as they represent a refuge, nursery
C. Lo Iacono and feeding ground for many species of crustaceans, fishes
National Oceanography Centre, University of Southampton and other groups (Husebo et al. 2002; Roberts et al. 2006,
Waterfront Campus, Southampton, UK

https://doi.org/10.1007/978-3-319-91608-8_26
272 A. Aymà et al.
2009; D’Onghia et al. 2010, this volume; Purser et al. 2013). To date, CWCs below 300 m have been reported in sev-
CWCs settle in seabed areas exposed to currents strong eral locations in the Mediterranean Basin (reviewed by
enough to prevent excessive sedimentation and carry food Lastras et al. 2016; Altuna and Poliseno, this volume). The
particles to sustain polyps and colonies (Frederiksen et al. occurrence of M. oculata and L. pertusa has been reported
1992; White et al. 2005; Dullo et al. 2008; Davies et al. down to 1100 m depth in Santa Maria di Leuca, at the mouth
2009). Such physical conditions often occur in escarpments, of the Adriatic Sea (Tursi et al. 2004; Mastrototaro et al.
seamounts and submarine canyons (Canals et al. 2006; 2010), and down to 600 m depth in the Bari Canyon, in the
Thiem et al. 2006; Kiriakoulakis et al. 2007), which southern Adriatic Sea (Freiwald et al. 2009; D’Onghia et al.
subsequently become key-habitats for the recruitment and 2010). In Sardinian canyons, M. oculata has been identified
maintenance of stocks of commercially exploited resources from 380 to 460 m depth, with occasional presence of L.
(Sardà and Cartes 1993; Cartes et al. 1994; Company et al. pertusa (Taviani et al. 2017). In the northwestern
2008). It should be kept in mind that the occurrence of large Mediterranean Sea, M. oculata has been found in the
submarine canyons deeply incising continental margin Cassidaigne Canyon, east of Marseille, from 200 m down to
segments adds heterogeneity to deep-sea habitats and an 1000 m, co-occurring with Corallium rubrum colonies in the
ecological complexity not yet fully explored (Canals et al. depth range of 200–325 m (Reyss 1970; Zibrowius 1980;
2013). Fiala-Medioni et al. 2012; Fabri et al. 2014). Also, Fanelli
Cold-water coral communities commonly occur in et al. (2017) recognised M. oculata from 525 to 575 m depth
marine waters with temperatures between 4 and 12 °C at Levante Canyon in the eastern Ligurian Sea, where small
(Freiwald et al. 2004). These temperatures can be found D. dianthus colonies were also identified. Dendrophyllia
between 50 and 1000 m depth at high latitudes and at cornigera was located within a narrow depth interval from
larger depths (up to 4000 m) at low latitudes (Roberts et al. 447 to 501 m in the Ionian Sea (Freiwald et al. 2009;
2006, 2009). In contrast, the Mediterranean Sea presents Mastrototaro et al. 2010) with D. dianthus occurring between
warmer deep water masses at 12–14 °C below the thermo- 425 and 1100 m in the same locations (Cairns 1995; Tursi
cline (i.e. at approximately 200 m depth; Borghini et al. et al. 2004; Mastrototaro et al. 2010).
2014), which results in limiting conditions for the growth In the North Catalan margin of the northwestern
of the majority of CWCs (Freiwald et al. 2004). This not- Mediterranean Sea these species have mostly been reported
withstanding, several species such as Madrepora oculata at shallower depths within submarine canyons. The upper
(Linnaeus, 1758), Lophelia pertusa (Linnaeus, 1758), flanks of Cap de Creus Canyon host healthy communities of
Desmophyllum dianthus (Esper, 1794) and Dendrophyllia M. oculata laying over patches of hard substrate at depths
cornigera (Lamarck, 1816) have been identified in the from 129 m down to 400 m and possibly deeper although not
Mediterranean Sea (Tursi et al. 2004; Hebbeln et al. 2009; inspected due to ROV operational limitations (Rossi et al.
Orejas et al. 2009; Mastrototaro et al. 2010; Gori et al. 2008; Orejas et al. 2009; Lastras et al. 2011; Lo Iacono et al.
2013; Rogers 2013; Angeletti et al. 2015; Lastras et al. 2012; Gori et al. 2013; Puig and Gili, this volume). Also,
2016; Addamo, this volume; Altuna and Poliseno, this vol- isolated colonies of L. pertusa, D. dianthus and D. cornigera
ume; Chimienti et al., this volume) (Table 26.1). Of these, have been found associated to M. oculata communities in the
M. oculata and L. pertusa are the most relevant CWC spe- same canyon (Orejas et al. 2009; Lo Iacono et al. 2012; Gori
cies in terms of abundance and biomass, forming large- et al. 2013; Puig and Gili, this volume). The recently explored
sized colonies that provide shelter, food and nursery to head of La Fonera Canyon revealed the presence of healthy
deep-sea fauna (D’Onghia et al. 2010, this volume; Rueda communities of M. oculata and D. cornigera at relatively
et al., this volume). The cosmopolitan D. dianthus is a soli- shallow water depth ranges, i.e. between 129 and 369 m and
tary species appearing in the Mediterranean Sea in associ- 131 and 325 m, respectively (Lastras et al. 2016). Again,
ation with L. pertusa and M. oculata (Pérès and Picard ROV operational limitations prevented exploration at larger
1964; Taviani et al. 2005; Reveillaud et al. 2008; Heindel depths. In the Lacaze-Duthiers Canyon head, L. pertusa and
et al. 2010; Addamo, this volume). In some circumstances, M. oculata were found at greater depths, ranging between
it can form pseudo-colonies with the skeletons of older 350 and 541 and 246 and 531 m, respectively (Gori et al.
individuals providing the substratum on which younger 2013; Lartaud et al. 2013).
individuals, including other CWC species, grow as In this study, we present the results of a thoughtful explo-
observed in banks off New Zealand and Chile (Squires ration of the deep reaches of large submarine canyons in the
1965; Cairns and Stanley 1982; Försterra et al. 2005, 2017; North Catalan margin thus providing, to our best knowledge,
Jantzen et al. 2013). the first in situ evidence about the presence of living speci-
26 Occurrence of Living Cold-Water Corals Within Submarine Canyons 273
Table 26.1 Recorded distribution, depth range (m) and sampling methods applied in different studies of cold-water coral species Lophelia per-
tusa, Madrepora oculata, Dendrophyllia cornigera and Desmophyllum dianthus in the Mediterranean Sea
Basin Location Depth range (m) Sampling method References
Lophelia pertusa
Ionian Sea SML 425–1100 Trawl hauls Tursi et al. (2004)
Ionian Sea SML 300–1100 ROV, dredges Taviani et al. (2005)
Ionian Sea SC 395–617 Trawl hauls Schembri et al. (2007)
Ionian Sea SML 520–1100 ROV, trawl hauls Carlier et al. (2009)
Ionian Sea SC 509–679 ROV Freiwald et al. (2009)
Ionian Sea SML 469–1100 ROV Mastrototaro et al. (2010)
Alboran Sea SoG 150–300 Grab sampling Álvarez-Pérez et al. (2005)
Alboran Sea MM 539–675 ROV Hebbeln et al. (2009)
NWMed NCM 100–400 ROV Lo Iacono et al. (2012)
NWMed NCM <400 ROV Gori et al. (2013)
NWMed GoL 531–554 ROV Fabri et al. (2014)
NWMed GoL 300–535 ROV Fiala-Medoni et al. (2012)
Madrepora oculata
Ionian Sea SML 300–1100 ROV, dredges Taviani et al. (2005)
Ionian Sea SC 509–679 ROV Freiwald et al. (2009)
Alboran Sea SoG 150–300 Grab sampling Álvarez-Pérez et al. (2005)
Alboran Sea MM 539–675 ROV Hebbeln et al. (2009)
NWMed GoL 210–510 Submersible Bourcier and Zibrowius (1973)
NWMed NCM 150 ROV Lastras et al. (2016)
NWMed GoL 300 Submersible, dredges Zibrowius (2003)
NWMed NCM 125 ROV Rossi et al. (2008)
NWMed NCM 180–300 ROV Orejas et al. (2009)
NWMed GoL 246–531 ROV Gori et al. (2013)
NWMed GoL 531–554 ROV Fabri et al. (2014)
NWMed NCM 129–369 ROV Lastras et al. (2016)
Ligurian Sea LC 540–545 ROV Fanelli et al. (2017)
Alboran Sea MM 622 ROV Hebbeln et al. (2009)
NWMed NCM 131–297 ROV Lastras et al. (2016)
GoL Gulf of Lion, LC Levante Canyon, MM Malaga mounds, NCM North Catalan margin, NWMed Northwestern Mediterranean margin, SML
Santa Maria di Leuca, SC Sicily Channel, SoG Strait of Gibraltar
mens of the solitary CWC D. dianthus down to 1400 m rine canyons in terms of new CWC occurrences, subse-
depth. This finding, together with the dead fragments of L. quently leading to a southward extension of the Gulf of Lion
pertusa and M. oculata retrieved at remarkable depths in the CWC province, which could be now re-named “Gulf of Lion
same area are of broad relevance for Mediterranean deep-sea and North Catalan canyons CWC province”.
ecology and highlight the interest of North Catalan subma-
274 A. Aymà et al.
26.2 Study Area 26.3 Materials and Methods
We inspected three large submarine canyons from the North 26.3.1 Data Collection
Catalan margin. Cap de Creus Canyon follows a WNW-ESE
direction, is 95 km long and ends at 2150 m depth (Amblas In summer 2011 the three canyons (Cap de Creus, La Fonera
et al. 2006). Its head is located 5 km northeast of the tip of and Blanes) were systematically inspected and sampled from
Cap de Creus coastal promontory. The 105 km long La north to south (Fig. 26.1) by using the research vessel
Fonera Canyon (also known as Palamos Canyon), has a N-S Sarmiento de Gamboa. Two complementary methods were
oriented head that leads to a NW-SE narrow and V-shaped applied: a remotely operated vehicle (ROV) and an Agassiz
upper course, followed by broader middle and lower reaches trawl (AGT) to respectively video-inspect and collect
that vanish at the base of the slope at 2540 m depth (Amblas biological samples from the bottom.
et al. 2006). The nearest shoreline is at only 0.8 km from the The ROV “Liropus 2000” was equipped with a HD
tip of the westernmost head branch of La Fonera Canyon Kongsberg OE 14-502A camera, with a horizontal resolution
(Lastras et al. 2011). Among the canyons investigated here, of 800 TV lines per picture height, a 1920 (H) × 1080 (V)
the southernmost one is Blanes Canyon, which extends picture elements video, and a 10 × optical zoom. Aligned to
along 180 km from its head, at less than 4 km from the near- the HD camera, the ROV had also a pair of parallel laser
est shoreline, to its mouth at 2600 m depth (Lastras et al. beams mounted 15 cm apart one from each other, which
2011). Blanes Canyon is roughly oriented N-S along its allowed measurements on the bottom including the sizing of
head, upper, and middle course, and then turns SE in its animals and other items in the imagery. Ten ROV video-
lower course, where some prominent meanders occur dives were conducted along transects at an approximated
(Amblas et al. 2006). height of 50–100 cm off bottom, and at low speed (up to 1.2
The closeness of the three canyon heads to the shoreline knots) (Table 26.2). The dives were performed along canyon
enhances their trapping ability of coastal and shelf flows axes in an upward direction, starting at 900, 1200, and
(Canals et al. 2013). All of them are able to capture dense 1500 m reference depths (Fig. 26.1). Other dives were carried
waters that form seasonally and escape from the continental out along a transect ascending the northern wall of La Fonera
shelf to the bathyal domain, carrying sediment, food, Canyon. The duration of the ROV video records was, on
pollutants and litter (Canals et al. 2006, 2013; Ulses et al. average, 113 min, resulting in a total of 19 h of faunal and
2008; Tubau et al. 2015), as well as sediment-laden flows geomorphological observations (Table 26.2).
that result from severe coastal storms (Palanques et al. 2005, In all dives oceanographic parameters known to directly
2006; Martin et al. 2006; Sanchez-Vidal et al. 2012). Of the affect the presence and growth of CWC colonies (Roberts
three inspected canyons, the most efficient one in trapping et al. 2006, 2009), such as salinity and temperature were
and conveying larger volumes of dense shelf water is Cap de continuously recorded by means of a SBE37 CTD installed
Creus (Ulses et al. 2008). All of them share abrupt heads and in the ROVs payload (Table 26.3). The benthic terrain
upper courses with steep walls where rocky outcrops and modelling tool (BTM) of ArcGis 10.2.1 software was used to
large boulders are common despite the dominant bottom calculate slope values from bathymetry data.
type is mud (Lastras et al. 2011). Canyon floors, where an We used an AGT to sample benthic fauna, as this tool
axial incision is occasionally observed, are rather flat and allows greater manoeuvrability in geomorphologically
usually sediment-covered. complex environments, such as canyons, than larger otter
The oceanography of the study area is characterised by trawling devices (i.e. the otter trawl Maireta System-OTMS,
the Northern Current, a steady mesoscale current flowing or commercial trawling nets) (Holme and McIntyre 1971).
south-westward over the outer shelf and slope where the The dredge was endowed with a 6 mm mesh size net, with
investigated submarine canyons are incised (Millot 1999). 2.5 × 1.2 m of horizontal and vertical opening, respectively.
The Northern Current has a baroclinic component from the AGT sampling was conducted 24 h after ROV dives, along
sea surface to approximately 400 m depth associated with a the axes of the three canyons, resulting in hauls at 900, 1200
shelf-slope density front that separates colder, fresher waters and 1500 m reference depths (Table 26.4). In total 8 AGT
over the continental shelf from warmer, saltier waters over hauls were performed in a down canyon direction, resulting
the outer continental margin and basin (Font et al. 1988). in a total swept area of 0.154 km2.
Fig. 26.1 (a) General location of ROV dives (D, red lines) and Agassiz trawl hauls (A, black lines) within (b) Cap de Creus, (c) La Fonera
and (d) Blanes submarine canyons of the North Catalan continental margin. (© GRC Geociències Marines, Universitat de Barcelona)
Table 26.2 Reference data for the ROV dives in terms of location and reference depth (700, 900, 1200 and 1500 m), date within year 2011, initial
and final transect location (latitude and longitude), duration of video record (min), depth range (m, from deeper to shallower as dives were per-
formed upwards) and swept area (m2)
Dive no. Location Date Initial location Final location min m m2 CWC Y/N
8 CCC-1500 axis 05/07 42°13′14″N 42°13′14″N 159 1570–1490 6456 N
03°48′48″E 03°48′48″E
9 CCC-1200 axis 05/07 42°16′53″N 42°17′25″N 97 1215–1200 5789 N
03°38′44″E 03°37′45″E
16 LFC-1500 axis 08/07 41°51′00″N 41°51′31″N 141 1570–1510 4136 N
03°24′25″E 03°23′59″E
18 LFC-1200 axis 09/07 41°51′53″N 41°05′03″N 119 1215–1155 3485 N
03°20′22″E 03°19′45″E
19 LFC-900 axis 09/07 41°52′25″N 41°52′49″N 83 985–860 2467 N
03°16′45″E 03°16′40″E
20 LFC-1500 lower N wall 09/07 41°51′30″N 41°52′48″N 238 1500–980 5582 Y
03°23′56″E 03°16′40″E
(continued)
276 A. Aymà et al.
Dive no. Location Date Initial location Final location min m m2 CWC Y/N
21 LFC-900 mid N wall 10/07 41°52′26″N 41°52′47″N 100 985–750 2063 N
03°23′57″E 03°23′55″E
23 LFC-700 upper N wall 10/07 41°54′10″N 41°53′46″N 150 730–600 2509 Y
03°16′09″E 03°16′09″E
31 BC-1500 axis 13/07 41°07′02″N 41°07′40″N 71 1520–1500 1870 N
02°52′50″E 03°52′44″E
32 BC-1200 axis 13/07 41°01′14″N 41°01′29″N 60 1225–1200 1892 N
02°50′45″E 02°50′42″E
33 BC-900 axis 13/07 41°04′15″N 41°04′31″N 68 910–900 1753 N
02°50′48″E 02°50′52″E
CCC Cap de Creus Canyon, LFC La Fonera Canyon, BC Blanes Canyon
Table 26.3 Mean values for temperature (T) and salinity (S) reported found. The software Image J was used to determine the area
for every dive frame by frame, by taking the known distance (15 cm)
Dive no. Dive T (°C) SD S (PSU) SD between the two ROV laser points that appeared on the imag-
8 CCC-1500 axis 13.15 0.029 38.41 0.007 ery as a reference, also assuming an averaged ROV constant
9 CCC-1200 axis 13.15 0.011 38.42 0.010 speed of 1.2 knots over the bottom. The separation between
16 LFC-1500 axis 13.17 0.004 38.40 0.029 the two laser points allowed, in addition, compensating for
18 LFC-1200 axis 13.15 0.002 38.42 0.028
ROV seabed height changes during navigation.
19 LFC-900 axis 13.21 0.009 38.44 0.019
20 LFC-1500 lower 13.16 0.008 38.47 0.004
Agassiz trawl samples were sorted on board, cleaned,
N wall counted, and finally weighted. Determining if well preserved
21 LFC-900 mid N wall 13.20 0.040 38.48 0.007 coral specimens collected with AGT were actually alive or
23 LFC-700 upper N 13.28 0.005 38.47 0.007 not was dubious. Therefore, the total weight of fragments
wall was used as a proxy for present or past biomass in each study
31 BC-1500 axis 13.17 0.003 38.45 0.002 area.
32 BC-1200 axis 13.15 0.002 38.45 0.003
33 BC-900 axis 13.24 0.004 38.45 0.003
SD standard deviation. For location codes and reference depths see
Table 26.2
26.4 Results
26.4.1 ROV Video-Observations

Table 26.4 Reference data for the Agassiz trawl (AGT) sampling sta-
tions, including location, depth range (m, from shallower to deeper as
trawls were performed downwards) and trawled area (m2)
The dense concentrations of CWCs found in the lower and
upper northern flank of La Fonera Canyon contrast with their
AGT no. Location m km2 CWC Y/N
absence in the ROV dives at Cap de Creus and Blanes can-
1 CCC-1500 axis 1408–1554 0.01009 N
2 CCC-1200 axis 1018–1236 0.01368 N
yons (Table 26.2). The living colonies of Desmophyllum
3 CCC-900 axis 771–880 0.00657 Y dianthus in La Fonera Canyon were particularly noticeable in
4 LFC-1900 axis 1526–2289 0.0152 N dives no. 20 (1400 m depth) and 23 (600 m depth) (Fig. 26.2a–
5 BC-1500 axis 1477–1569 0.00584 N c), being dive no. 20 the only one conducted across the can-
6 BC-1200 axis 1204–1424 0.00627 Y yon wall (Fig. 26.2b). In this transect, seabed slope values
7 BC-900 axis 752–864 0.09237 Y were ranging from 16° to 30°. CWC individuals were identi-
8 BC-1100 open 1063–1159 0.00602 N fied on a 10 m high rock step with slope values of 16°, within
slope
the 1420–1400 m depth range. Dive no. 23 was conducted at
For location codes and reference depths see Table 26.2 680 m depth along the canyon axis (Fig. 26.2c), and, in con-
trast with dive no. 20, slope values were less than 6°.
26.3.2 Video and Hauling Data Treatment Hundreds of D. dianthus specimens grouped in several
clusters of different sizes (i.e. up to several tens of recogni-
Video footage from ROV was analysed in slow motion (i.e. sable individuals) were found along dive no. 20 (Fig. 26.3a),
at 50% of the recording speed). CWC individuals’ identifica- settling on a vertical rocky wall. Most corals were hanging
tion was resolved to the lowest possible taxonomical level from the rocky outcrop with their calyx looking either down
whereas the associated fauna was identified at genus level. or sideward. Many of them were observed as inhabiting rock
The software ArcGis 10.2.1 allowed calculating the length of protrusions and bumps with no or little soft sediment on top
the different sections in each transect where colonies were (Fig. 26.3b). The spaces in between coral clusters or sparse
Fig. 26.2 (a) Location of the ROV dives (D) in La Fonera Canyon where living cold-water corals (CWCs) were observed. 3-D plots show the
precise location of dives 20 (b) and 23 (c). Red segments indicate the location of CWCs. (© GRC Geociències Marines, Universitat de Barcelona)
Fig. 26.3 (a) ROV video capture showing Desmophyllum dianthus in thus clusters lying on a soft muddy bottom at the foot of the escarpment
a rock outcrop in La Fonera canyon at 1409 m depth. (b) D. dianthus after detachment from the outcrop. Distance amongst green laser dots is
specimens attached to a near-vertical rock outcrop. (c) and (d) D. dian- 15 cm. (© GRC Geociències Marines, Universitat de Barcelona)
individuals were just barren rock. Detached coral clusters of D. dianthus specimens (Fig. 26.4b). In ROV imagery deca-
were also found settling onto the soft bottom at the base of pod crustaceans, echinoids, anemones and holothurians were
the escarpment (Fig. 26.3c, d). observed between coral clusters attached to the outcrop.
Individuals of D. dianthus were also located attached to a Holothurians, identified as Holothuria forskali, were the most
rocky outcrop during dive no. 23 (Fig. 26.4a). Again, hun- abundant group, followed by echinoids, all belonging to
dreds of individuals were detected hanging with their calix genus Gracilechinus. Decapod crustaceans identified as
looking downward or sideward. This ROV transect presented Munida sp. were observed sheltering in spaces between coral
higher density values of D. dianthus individuals than dive no. aggregations. Actiniae were the less abundant group. Also,
20. Specimens formed aggregations, resting on a vertical hard we noticed the presence of several specimens belonging to
substrate with vertical slope and also in places where soft classes Polychaeta and Bivalvia, but it was not possible iden-
sediment accumulated. We detected associated fauna amidst tifying them at the species level on the video imagery.
278 A. Aymà et al.
Regarding temperature and salinity, similar mean values were

observed between canyons, and differences between dives were
also very small (see Table 26.3). For dives D20 and D23, where
CWCs occurred, mean temperature values were 13.16 ± 0.01 °C
and 13.28 ± 0.01 °C, respectively. The same salinity mean value
was recorded in both dives (38.47 ± 0.01 PSU).
26.4.2 Agassiz Trawling
Agassiz trawl sampling yielded three species of CWCs:

Lophelia pertusa, Madrepora oculata and D. dianthus
(Fig. 26.5). In Blanes Canyon where all the three species were
present, L. pertusa was sampled at trawl 7 (752–864 m) yield-
ing 11.477 g, M. oculata at trawl 6 (1204–1424 m) with
244 g, and D. dianthus at both trawls and depths, with 1084
and 2050 g, respectively (Fig. 26.1 and Tables 26.4 and 26.5).
Weight of L. pertusa per unit area for trawl 7 was 124.3 kg/
km2, while D. dianthus presented higher values at the deeper
trawl 6 than at the shallower trawl 7 (i.e. 326.9 kg/km2 vs.
11.7 kg/km2). At trawl 7, the weight of M. oculata per unit
area was about 39 kg/km2 (Table 26.5).
The solitary coral D. dianthus was also sampled in Cap de
Creus Canyon by AGT at trawl 3 from 771 to 880 m of water
depth, with 3 g and an estimated weight of 0.46 kg/km2. Such
isolated occurrence of D. dianthus was also observed with
ROV on rock escarpments in La Fonera Canyon at 1400 and
Fig. 26.4 Desmophyllum dianthus community at 680 m of water depth 680 m depth. By contrast, in Blanes Canyon, D. dianthus
in La Fonera canyon. (a) ROV video screenshot showing a number of appeared in association to M. oculata at 1200 m depth in
individuals settling on a vertical to overhanging rock outcrop with their
calyxes looking downwards. (b) Living echinoderms and holothurians
trawl 6, and with L. pertusa at 900 m depth in trawl 7
associated to the D. dianthus community. (© GRC Geociències (Table 26.4). Some specimens of L. pertusa recovered from
Marines, Universitat de Barcelona) Blanes Canyon in trawl 7 also had associated fauna, mainly
polychaetes.
Fig. 26.5 Fragments of

cold-water corals retrieved by
Agassiz trawling. (a)
recovered in Agassiz trawl 7
(752–864 m depth) within
Blanes Canyon. (b) and (c)
Madrepora oculata and
Lophelia pertusa recovered in
Agassiz trawl 6 (1204–
1424 m depth) within Blanes
canyon. Scale bars: 1 cm. (©
GRC Geociències Marines,
Universitat de Barcelona)
Interaction between CWC and marine litter was observed 1400 m (Fig. 26.7). Previously, only one single specimen of
in samples retrieved from AGT 7 (752–864 m depth) in D. dianthus had been reported after retrieval by trawl hauling
Blanes Canyon. There, a noticeable L. pertusa colony had at 1758 m in the Balearic Basin, although it is unclear if it
grown around and over nylon ropes from an old net was dead or alive (Cartes et al. 2009).
(Fig. 26.6). Our video images show colonies of D. dianthus attached
to a rock outcrop, evidencing that these are not dead colo-
nies drifted by the currents. Similarly, Jantzen et al. (2013)
26.5. Discussion and Försterra et al. (2017) in Chilean waters, as well as
Fourt et al. (this volume), in the canyons of the Gulf of Lion,
Living colonies of Madrepora oculata and Lophelia pertusa in the northwestern Mediterranean Sea, also observed colo-
in the northwestern Mediterranean Sea had been previously nies of D. dianthus in downward and sideward positions in
reported between 180 and 400 m depth in Cap de Creus deep water locations, similar to those observed in our study.
Canyon by Rossi et al. (2008), Orejas et al. (2009), and Gori By contrast, M. oculata and L. pertusa did not present polyp
et al. (2013) and down to 400 m depth by Lo Iacono et al. tissue or any other evidence that allow us to confirm that the
(2012) and Gori et al. (2013), mostly on hard substrata specimens sampled with AGT were alive. Whereas more
(Fig. 26.7) (see also Altuna and Poliseno, this volume; data would be required to corroborate the occurrence of liv-
Chimienti et al., this volume; Fourt et al., this volume). M. ing specimens of both corals, the good state of preservation
oculata had also been reported at shallower depths (i.e. of individuals, together with the fact that L. pertusa was
155 m) in La Fonera Canyon (Lastras et al. 2011, 2016) retrieved as growing on a nylon wire (as a proxy of age),
(Fig. 26.7). suggest that living deep-sea corals likely occur in the can-
Our findings in the North Catalan canyons constitute the yon axis, or at least inhabited this environment in very
deepest confirmed record in the entire Mediterranean Sea for recent times. Our findings for M. oculata and L. pertusa
Desmophyllum dianthus, which was found at depths below colonies are of relevance, as they could point out to a pos-
sible extension of the currently known distribution range of
the species in the western Mediterranean Sea, down to 1200
Table 26.5 Biomass of cold-water coral species retrieved in Agassiz and 900 m depth, respectively (Fig. 26.7). In the investi-
trawls (AGT) in terms of total weight (kg) and estimated biomass (kg/km2) gated depths of the studied canyons, the retrieved fragments
Species AGT no. Location kg kg/km2 of colonies showed that M. oculata and L. pertusa did not
Madrepora oculata 6 BC-1200 axis 0.244 38.92 appear associated to each other but with D. dianthus, which
Lophelia pertusa 7 BC-900 axis 11.477 124.25 is another frequent contributor to CWC communities (Pérès
Desmophyllum 3 CCC-900 axis 0.003 0.46
dianthus
and Picard 1964).
Desmophyllum 6 BC-1200 axis 2.050 326.95 Beyond our study area, living CWCs in the Mediterranean
dianthus Sea have been identified off Thassos Island in the Aegean
Desmophyllum 7 BC-900 axis 1.084 11.74 Sea, the southern Adriatic, the Ionian Sea, the Sicily
dianthus Channel, the Tyrrhenian Sea, the Ligurian Sea, the Gulf of
For location codes and reference depths see Table 26.2 Lion and the Strait of Gibraltar (Freiwald et al. 2009; Taviani
Fig. 26.6 (a) Fragments of a Lophelia pertusa colony growing on and surrounding nylon net cords retrieved from Agassiz trawl 7 (752–864 m
depth) in the Blanes Canyon. (b) Detail of frame (approximate) in A (© GRC Geociències Marines, Universitat de Barcelona)
280 A. Aymà et al.
Fig. 26.7 Location of all CWCs species reported in the study area. (a) Madrepora oculata, Dendrophyllia cornigera and Corallium rubrum
General bathymetry of Cap de Creus Canyon. (b) Zoom in of the head occurrences reported by Rossi et al. (2008), Orejas et al. (2009), Lo
and upper course of Cap de Creus Canyon, and adjacent continental Iacono et al. (2012), Gori et al. (2013), and Lastras et al. (2016). White
shelf, showing cold-water coral (CWC) occurrences. (c) General areas: new locations of CWCs found in this study from ROV imaging.
bathymetry of La Fonera Canyon. (d) Zoom in of the head and upper- White lines: Agassiz trawling lines along which CWCs were sampled in
middle course of La Fonera Canyon, and adjacent continental shelf, this study. The new results obtained extend the range of CWC occur-
showing CWC occurrences. (e) General bathymetry of Blanes Canyon. rences in the submarine canyons of the northwestern Mediterranean Sea
(f) Zoom in of the head and upper-middle course of Blanes Canyon, and and in the entire basin. (© GRC Geociències Marines, Universitat de
adjacent continental shelf, showing CWC occurrences. Magenta areas: Barcelona)
et al. 2017; Fanelli et al. 2017; Chimienti et al., this volume; et al. 2004), a depth that is some hundreds of meters shal-
D’Onghia, this volume). In these locations CWCs usually lower than the deepest canyon reaches explored in our study.
occur along the continental shelf edge, on sea knolls and The fauna associated to the CWC species here investi-
seamounts, and within canyons. The deepest known occur- gated belongs to different taxonomic groups, i.e. decapods
rence of CWCs among all these locations is in Santa Maria (Munida sp.), holothurians (Holothuria forskali) and echino-
di Leuca, where the framework-building species M. oculata derms (Gracilechinus sp.), with the most abundant speci-
and L. pertusa, commonly in association with solitary corals mens from classes Bivalvia and Polychaeta. A detailed study
such as D. dianthus, have been detected at 1100 m (Tursi in Santa Maria di Leuca (Mastrototaro et al. 2010) identified
more than 200 species living together with CWCs, where firm if the sampled corals were alive. In any case, the growth
Bivalvia and Polychaeta, together with Crustacea and of some of these colonies on nylon nets points to the exis-
Echinodermata, were also among the most important groups tence of living colonies nearby and/or in very recent times.
contributing to local biodiversity. A rather small number of Our findings illustrate the relevance of CWC communities in
other studies in the Mediterranean have also considered the investigated canyon systems. Following previously pub-
CWCs’ associated fauna, such as Tunesi et al. (2001), lished records of CWCs at generally shallower water depths,
Schembri et al. (2007), Mastrototaro et al. (2010), Lastras our study evidences how CWC occurrences can be extended
et al. (2016), D’Onghia (this volume), and Rueda et al. (this deeper in submarine canyons of the northwestern
volume). Mediterranean Sea. Our results finally show the relevance of
Our data highlight the capability of CWCs to form the North Catalan canyons in the frame of an improved
aggregations and colonies at great depths under current knowledge of deep-sea benthic communities and particularly
environmental conditions in the northwestern CWCs in the Mediterranean Sea. This added knowledge
Mediterranean Sea. In the three investigated submarine should be used to design future management and conserva-
canyons, where we detected the presence of CWCs, a tion strategies.
higher energy hydrodynamic regime occurs in comparison
to open slopes at equivalent depths, especially during Acknowledgements The work presented here was developed within
intense transport episodes driven by atmospheric forcing the DOS MARES (ref. CTM2010-21810-C03) research project funded
by the Spanish Government, and the PROMARES-OASIS DEL MAR
(Canals et al. 2006; Sanchez-Vidal et al. 2012; Durrieu de research cruise funded by Obra Social “la Caixa”. The final push to
Madron et al. 2013). The funnelling of matter (and energy) finalise this paper was given by IDEM project (ref. 11.0661/
from shallow to deep (Canals et al. 2004) along submarine 2017/750680/SUB/ENV.C2), funded by DG Environment of the
canyons provides an above-threshold food flux for benthic European Commission and project I-MarCat funded by Institut
d’Estudis Catalans. Support was also received from Generalitat de
resident species, in which flow velocity and food particle Catalunya autonomous government through “Grups de Recerca
concentration look essential to the sustenance of the corals Reconeguts” grant 2017 SGR 315 to GRC Geociències Marines. A
and associated species (Guinotte et al. 2006; Roberts et al. Mecho is supported by the Ecology and Sustainable Management of
2006, 2009; Cairns 2007; Davies et al. 2009; Purser et al. Oceanic Islands (ESMOI), a Millennium Institute/Nucleus (code:
120030) supported by the Millennium Scientific Initiative of the
2010; Puig and Gili, this volume). In parallel, the episodic Ministry of Economy, Development and Tourism from Chile.
high speed of near-bottom currents removes sediment that
could eventually suffocate the organisms, thus easing coral
growth. For instance, current speeds in the range of
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Drop Chapter
Submarine Canyons in the Mediterranean: 27
A Shelter for Cold-Water Corals
Pere Puig and Josep-Maria Gili
Abstract systems (Shepard and Dill 1966; Harris and Whiteway 2011;
In the Mediterranean Sea, many of the locations where Harris et al. 2014). They evolve over geological timescales
cold-water coral communities have been reported and acting as preferential conduits of sediment from coastal and
documented tend to be associated to submarine canyon shelf environments to adjacent deep-sea basins, involving
environments. This contribution provides a summary of different sediment transport processes and triggering mecha-
the Mediterranean canyons where, up to date, cold-water nisms operating at various time-scales (Shepard 1981; Piper
corals develop, describing the most common species, and Normark 2009; Puig et al. 2014).
their water depth distribution and degree of preservation, Submarine canyons, by dissecting continental margins,
and the prevalent hydrodynamic forcing at specific sites. create a bathymetric steering of oceanic circulation and
Considering that the inventory, characterisation and enhance shelf-slope exchange processes. The specific local
detailed mapping of Mediterranean submarine canyons is circulation around canyon heads promote upwelling of cold,
far from complete, this compilation urges to focus new nutrient-rich waters to the sea surface that enhance surface
research and exploration efforts on these morphological productivity (Allen and Durrieu de Madron 2009), internal
features, as they appear to act as natural shelters of cold- waves tend to be focused along canyon axis creating local-
water coral communities at present times. ised mixing and particle resuspension and advection
(Shepard et al. 1979; Gardner 1989), and dense waters gen-
Keywords erated over shelves mainly cascade trough submarine can-
Shelf-slope exchange · Dense shelf water cascades · yons, delivering large amount of particulate and dissolved
Internal waves · Canyon head · Rocky outcrop organic and inorganic matter from shallow to deep-sea envi-
ronments (Canals et al. 2006).
In general, due to their specific hydrodynamics, submarine
The true extent of the cold-water coral (CWC) communities canyons exhibit larger particulate organic matter fluxes than
in the Mediterranean Sea is still poorly known, and the rela- the adjacent open slope areas and, therefore, act as hotspots of
tively few verified records of live colonies exhibit a scattered benthic biodiversity (Vetter 1994; Vetter and Dayton 1998;
distribution pattern rather than a belt of occurrences, as is the Bosley et al. 2004; De Leo et al. 2010). Additionally, shelf-
case in the Northeast Atlantic (Zibrowius 1980; Freiwald incising canyons are characterised by steep terrains, contain-
et al. 2009; see Chimienti et al., this volume). Indeed, a coming vertical to overhanging bedrock exposures, which create
mon characteristic of Mediterranean CWC is that several of important habitats for benthic ecosystems where biologically
the reported sites are associated to submarine canyon envi- diverse communities, including CWC, may settle and develop
ronments, and therefore, their occurrence in some (e.g. Orejas et al. 2009; De Mol et al. 2010; Huvenne et al.
Mediterranean regions appears to be governed by the pres- 2011; Gori et al. 2013; see Rueda et al., this volume).
ence of such seafloor morphologies. Nonetheless, submarine canyons also provide refuge to a
Submarine canyons are common geomorphic features number of species of commercial interest (Company et al.
that occur worldwide on passive and active continental mar- 2012) and, as they tend to be targets of intense fisheries, many
gins, as single features or arranged in hierarchic tributary of these benthic habitats are severely damaged or under threat
(see Otero and Marin, this volume).
P. Puig (*) · J.-M. Gili The Mediterranean Sea is characterised by some remark-
Institute of Marine Sciences (CSIC), Barcelona, Spain ably young submarine canyons (Pliocene-Quaternary),

https://doi.org/10.1007/978-3-319-91608-8_27
286 P. Puig and J.-M. Gili
although several of them are much older and inherited from ume). This fact may suggest the presence of these two spe-
the lowering of sea level during the Messinian salinity crisis cies in the Catalan margin submarine canyons at deeper
ca. 5.5 Ma (million years ago). In comparison to their oce- locations than those previously explored with ROV dives.
anic counterparts, canyons in the Mediterranean Sea have At the eastern sector of the Gulf of Lions canyoned margin,
been described as more dendritic and closely spaced, steeper, large colonies of M. oculata have been also reported in
shorter and with a smaller depth range (Harris and Whiteway Cassidaigne Canyon (Bourcier and Zibrowius 1973; Watremez
2011). In particular, the northwestern Mediterranean (i.e., 2012; Fabri et al. 2014, 2016) and small patches of M. oculata
the Ligurian, Gulf of Lions and Catalan margins) is charac- have been recently reported in Bourcart (also hosting D. cor-
terised by a dense network of submarine canyons (Canals nigera), Sicié and Var submarine canyons (Fabri et al. 2014),
et al. 2004; Migeon et al. 2012). It was in this region, specifi- being all of those encounters at depths ranging from 200 to
cally in the Cap de Creus and Lacaze-Duthiers submarine 350 m. A comprehensive list of submarine canyon locations in
canyons, where the first occurrences of living CWC commu- this Mediterranean region hosting CWC communities is pro-
nities in the Mediterranean were reported (Pérès and Picard vided by Fourt et al., this volume. Further East, in the Ligurian
1964; Reyss 1964a, b). More recent surveys in these two Sea, living M. oculata was also reported by Tunesi et al. (2001)
canyons using remotely operated vehicle (ROV) and manned at a 210 m water depth cliff off Portofino promontory, presum-
submersible have provided more accurate and quantitative able in a canyon head region of a tributary of Levante Canyon
investigations of CWC distribution (Orejas et al. 2009; (see Figure 2 in Migeon et al. 2012).
Watremez 2012; Gori et al. 2013; Fabri et al. 2014; Fourt The southwestern Adriatic Sea is another Mediterranean
et al. this volume). Madrepora oculata is the most abundant region where dense shelf cascades occur (Zoccolotti and
CWC in both canyons, while Lophelia pertusa and Salusti 1987; Trincardi et al. 2007). There, the Bari Canyon
Dendrophyllia cornigera mostly occurs as isolated colonies channelises most of the dense water flows (Turchetto et al.
or in small patches. An important exception was detected in 2007) and it also harbors live CWC communities (Freiwald
a vertical cliff in Lacaze-Duthiers Canyon where a large L. et al. 2009; Angeletti et al. 2014; Angeletti et al., this vol-
pertusa framework has been documented (Gori et al. 2013; ume). Colonies of L. pertusa, M. oculata and D. cornigera
Fourt et al., this volume). In both canyons, coral populations (few isolated) have been reported in this canyon at slightly
are distributed in a depth range of 180–550 m, although deeper locations (300–640 m water depth) than those in the
deeper areas have not been explored yet, and are dominated northwestern Mediterranean canyon head regions. Further
by medium and large colonies. The frequent presence of South along the western Adriatic margin, in a canyoned
small-sized colonies also indicates active recruitment (Gori region off Otranto and Tricase, living specimens of L. per-
et al. 2013). These submarine canyons are affected by the tusa and M. oculata where retrieved from blocks and thin
periodical arrival of dense shelf water cascades (Palanques hardgrounds at the canyon’s base (720–790 m water depth)
et al. 2006; Canals et al. 2006; Puig et al. 2008), which con- using grab sampling (Angeletti et al. 2014). These authors
tribute to create a favorable environment (i.e. exposed bed- pointed out that these new findings suggest an almost unin-
rocks and large organic particle fluxes) within the canyon terrupted, albeit patchy, belt of CWC sites all along the
heads for CWC settling and growing (Fig. 27.1). south-western Adriatic margin from Bari to Otranto, con-
Slightly towards the South, in the neighboring La Fonera necting the Adriatic populations to the well-known Ionian
Canyon (Catalan margin), an extensive ROV survey has Santa Maria di Leuca CWC province (Freiwald et al. 2009),
recently documented the presence of CWC communities on following the outflow of Adriatic Deep Water.
different canyon-head tributaries and environments (Lastras In the southeastern side of the Adriatic, Angeletti et al.
et al. 2016; Lastras et al., this volume). In general, larger and (2014) also reported two CWC sites located in submarine
healthier M. oculata colonies in this canyon are located in canyons indenting the Montenegrin slope at depths between
the rougher rocky areas of the canyon walls with higher 420 and 490 m (see also Angeletti et al., this volume). ROV
slope gradients. They span over water depths of 130–370 m, surveys revealed that rocky outcrops in this canyoned region
being most frequent between 180 and 300 m depth. D. corni- are used as substrate for the settlement of large colonies
gera is found in a slightly similar water depth range, but (>1 m in height) of M. oculata, in addition to small colonies
preferentially settles on moderately sloping seafloor with of L. pertusa and clusters of D. cornigera.
rocky outcrops and also in areas partially covered with sedi- A new Mediterranean CWC province has been recently
ments. In contrast with the neighboring Cap de Creus and identified south of Sardinia Island after ROV dives in Nora
Lacaze-Duthiers canyons, L. pertusa appears to be absent in Canyon (Taviani et al. 2016). This canyon harbor dense coral
the explored areas of La Fonera Canyon. However, Agassiz colonies of M. oculata that have been observed between 380
trawl samples in the neighboring Blanes Canyon collected and 460 m depth, but also contains occasional presence of L.
presumably living M. oculata and L. pertusa colonies at pertusa and D. cornigera. Large arborescent bushes of M.
1200 and 900 m depth, respectively (see Aymà et al., this vol- oculata growing of dead coral frames surrounded by muddy
27 Mediterranean Submarine Canyons: A Shelter for Cold-Water Corals 287
Fig. 27.1 (a) High-resolution

bathymetric map (5 m grid) of
the Cap de Creus continental
shelf and submarine canyon
head showing the rough
terrain on its upper reaches
where CWC communities
develop. (b) Photography of
Madrepora oculata colonies
on the southern flank of the
canyon at 250 m water depth
obtained during a dive of the
submersible JAGO
(copyright: IFM-GEOMAR/
ICM-CSIC). See location (red
star) in (a). The inset map of
the western Mediterranean in
(a) also shows the locations of
the submarine canyons
mentioned in the text (ordered
as they have been introduced):
1: Cap de Creus and Lacaze
Duthiers; 2: La Fonera and
Blanes; 3: Cassidaigne; 4:
Bourcart; 5: Sicié; 6: Var; 7:
Levante (off Portofino); 8:
Bari; 9: canyons off Otranto
and Tricase; 10: Montenegrin
canyons; 11: Nora; 12:
Minorca and canyons off
Formentor; 13: La Linea and
Guadiaro
sediments with abundant coral rubble are commonly found So far, more than 800 examples of large canyon systems
in this canyon environment. have been counted by Harris et al. (2014) for the Mediterranean
The ROV dives conducted by Oceana in Minorca Canyon Sea using Shuttle Radar Topography Mapping (SRTM30_
(Balearic Islands), also documented the presence of D. cornig- PLUS) 30-arc second database. The inventory of Mediterranean
era on several locations along the explored canyon head region submarine canyons is far from complete as it largely depends
(Marin and Aguilar 2012). More recent ROV surveys in the on the resolution of the available detailed bathymetry. In
Balearic margin by Grinyó et al. (2018) confirmed the presence recent years, national and international programs have funded
of numerous colonies of D. cornigera in Minorca Canyon as acquisitions of new higher-resolution morphological data
well in the upper reaches of the submarine canyons developed allowing canyon systems never observed before to be identi-
on the steep slope off Formentor Cape (Majorca Island), which fied (see examples in Würtz 2012; CIESM 2015). Given that
were mainly found between 120 and 200 m water depth. ROV several of the reported CWC sites in the Mediterranean Sea
dives off Formentor Cape also found sparse colonies of M. ocu- have been documented in steep and rough submarine canyon
lata at 300 m water depth (Grinyó et al. 2018). environments, it would be reasonable to focus the new research
In the western Alborán Sea, close to the Strait of Gibraltar, efforts on these morphological features once properly mapped,
Vázquez et al. (2015) reported the presence of colonies of as they appear to act as natural refuges of Mediterranean CWC
M.oculata and D. cornigera in La Linea and Guadiaro subma- at present times. The distribution (density and aggregation of
rine canyons. In this Mediterranean region, the hydrodynamics colonies) and d emography of coral population could be a good
within the canyon is mostly dominated by semidiurnal internal indicator of the degradation or preservation of CWC commu-
tides (García Lafuente et al. 1999; Puig et al. 2004), which nities in the canyons, parameters that should be used to pro-
also seem to create favorable conditions for CWC communi- pose appropriate measures for the protection and management
ties’ development. of submarine canyons areas.
288 P. Puig and J.-M. Gili
Acknowledgements Multibeam bathymetric data shown in Fig. 27.1a (Menorca Channel, Western Mediterranean Sea). Progr Oceanogr
was kindly provided by the Spanish Fishery General Secretary (shelf) 162:40–51
and Fugro Survey Ltd. and AOA Geophysics Inc. (canyon). We thank Harris PT, Whiteway T (2011) Global distribution of large submarine
Ruth Durán for her help with the bathymetric data integration and the canyons: geomorphic differences between active and passive conti-
mapping representation. This contribution benefited from the remarks nental margins. Mar Geol 285:69–86
and comments made by the Editor, Covadonga Orejas, and the review- Harris PT, Macmillan-Lawler M, Rupp J, et al (2014) Geomorphology
ers Marie Claire Fabri and Andrea Gori to whom we are also grateful. of the oceans. Mar Geol 352:4–24
Huvenne VAI, Tyler PA, Masson DG, et al (2011) A picture on the wall:
innovative mapping reveals cold-water coral refuge in submarine
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Drop Chapter
A Cold-Water Coral Habitat in La Fonera 28
Submarine Canyon, Northwestern
Mediterranean Sea
Galderic Lastras, Anna Sanchez-Vidal, and Miquel Canals
Abstract Dendrophyllia cornigera have been reported at the head and

Based on remotely operated vehicle video imaging, we upper flanks of Cap de Creus canyon (Orejas et al. 2009; Puig
describe a cold-water coral habitat in La Fonera canyon and Gili, this volume) at depths ranging between 200 and
head (northwestern Mediterranean Sea) and the human 300 m, and at deeper locations in the Lacaze-Duthiers canyon
impacts which threat this habitat. The dominant cold- (250–530 m) and the Cassidaigne canyon (200–1000 m)
water coral species is Madrepora oculata along with (Gori et al. 2013; Fabri et al. 2014; Fourt et al., this volume).
Dendrophyllia cornigera. The first occur on highly slop- Recently, Lastras et al. (2016) revealed the extensive presence
ing rocky outcrops most frequently between 180 and of CWCs in La Fonera canyon (Fig. 28.1), located immedi-
300 m water depth, being the largest colonies those pro- ately south of Lacaze-Duthiers and Cap de Creus canyons.
tected by topographic overhangs. Predictive modelling La Fonera canyon cuts through the North Catalan margin
accounting for terrain morphology and positive observa- for 110 km from its head at 60–130 m depth down to 2550 m
tions indicates that cold-water coral habitat extent should water depth. The head of the canyon incises 28 km into the
span over many areas of the canyon head, but M. oculata shelf following a WNW-ESE trending course, with a N-S ori-
is mostly absent in the canyon branches incised closer to ented shallowest part (Lastras et al. 2011). Pervasive networks
the coastline. This could be a consequence of an excess of of gullies carve its southern highly sloping wall (>25°),
sediment arrival during eastern storms. Daily trawling whereas daily trawling activity has smoothed the northern
activity also results in enhanced sediment fluxes, which wall at depths shallower than 800 m (Puig et al. 2012). High
could account for some M. oculata colonies partially cov- resolution bathymetry data show that the head consists of
ered by fine mud in the eastern wall of the canyon. Recent three main branches (Fig. 28.1a): Cap de Begur branch, which
physical damage is also observed at specific locations. runs in a N-S direction and has its tip at 135 m water depth; Illa
Negra branch, which is NW-SE oriented and has its tip at 60 m
Keywords water depth at a distance of barely 800 m from the coastline;
Cold-water coral · Madrepora oculata · Dendrophyllia and Sant Sebastià branch, which is W-E oriented and has its tip
cornigera · Submarine canyon · Remotely operated at 90 m water depth; as well as by many minor gullies.
vehicle · Anthropogenic impact Contrasting terrain characteristics along the canyon walls are
indicative of changing basement lithology, from rough, highly
sloping outcropping granitoids along Illa Negra and Sant
Cold-water corals (CWCs) have been observed in different Sebastià branches, to smoother, layered sedimentary outcrop-
canyons of the northwestern Mediterranean Sea, mainly by ping strata along the eastern wall of Cap de Begur branch.
means of remotely operated vehicles (ROV) (see Puig and A systematic exploration of the different environments
Gili, this volume). Madrepora oculata, Lophelia pertusa and within La Fonera canyon head aiming at detecting CWC
communities and quantifying their extent was performed by
G. Lastras (*) · M. Canals
means of 21 ROV dives in 2009 and 2010, using a Seaeye
GRC Geociències Marines, Departament de Dinàmica de la Terra i
de l’Oceà, Facultat de Ciències de la Terra, Universitat de Lynx 1500 operated from Motor Vessel (MV) Bon Pigall
Barcelona, Barcelona, Spain owned by Fundació Argomaris. Dive transects summed up a
e-mail: [email protected] total distance of 11.09 km, surveyed between 79 and 401 m
A. Sanchez-Vidal depth. ROV images display a noticeable habitat variety, in
GRC Geociències Marines, Universitat de Barcelona, terms of bottom topography and substrate types. These habi-
Barcelona, Spain

https://doi.org/10.1007/978-3-319-91608-8_28
292 G. Lastras et al.
Fig. 28.1 Cold-water corals

in La Fonera canyon head. (a)
Bathymetric map of the
canyon head with indication
of (1) M. oculata
observations, (2) possible
lateral extension of observed
CWC colonies according to
maximum entropy modelling
and negative observations, (3)
location of selected ROV
images in (b–d). See location
in inset. LFC La Fonera
canyon head. Scale bars are
approximate. (© GRC
Geociències Marines,
Universitat de Barcelona)
tats mainly include rocky outcrops and large boulders, sandy where, although less densely, they extend further south
(coarse sand to fine gravel mixture) bottoms and fine (clay to (Fig. 28.1). Contrarily, M. oculata colonies are much
medium sand mixtures) sediment-covered bottoms, from scarcer, smaller and more isolated along the Illa Negra
flat, homogeneous sediment-covered seafloor to near-vertical branch, and have not been observed at all along Sant
and over-hanging rock walls with small holes and caves. Sebastià branch. Medium-sized highly-impacted living
The dominant CWC species in La Fonera canyon head is colonies develop along the middle and upper sections of
M. oculata (Fig. 28.1b–d), often accompanied by other spe- the western wall of Illa Negra branch, nearby the conflu-
cies including the gorgonians Eunicella cavolinii and ence with Cap de Begur branch (Fig. 28.1).
Corallium rubrum, the scleractinian corals D. cornigera and Predictive modelling of CWCs occurrence in La Fonera
Caryophyllia smithii, as well as sponges, hydrozoans, bryo- canyon head by maximum entropy modelling results in an
zoans and the bivalve Neopycnodonte cochlear frequently area of 0.36 km2 having over 70% probability of M. oculata
forming dense clusters. Mobile species roaming over or occurrence, with 0.10 km2 exceeding 80% probability
between the corals include the spiny lobster Palinurus ele- (Lastras et al. 2016). This modelling, based solely on terrain
phas, the squad lobster Munida sp., hermit crabs, sea urchins, morphology and positive CWCs observations, clearly over-
sea cucumbers and octopuses. Dense populations of the estimates coral occurrence in Illa Negra and Sant Sebastià
ophiurioid Ophiothrix sp. have been observed attached to branches. This indicates that there are differences between
coral branches. the three branches that control the presence of CWCs which
The CWCs are not homogeneously distributed within are not accounted for in the model. Such factors could be
the different La Fonera canyon environments (Lastras either limiting in Illa Negra and Sant Sebastià branches, or
et al. 2016), but occur mainly on rocky outcrops and large favouring in Cap de Begur branch, namely food (i.e. organic
boulders, as well as on fine sediment-covered bottoms matter) availability, suspended sediment concentration and/
where some objects act as substratum (e.g. pebbles, fishing or hydrodynamics. The dramatic incision of La Fonera can-
lines). M. oculata colonies occur most frequently between yon, with its head tip located at so short distance from the
180 and 300 m water depth (mean 230 m) on highly slop- coastline, could explain, at least in part, this mismatch
ing areas (mean 42.8°). They generally form apparently between what is predicted by the model and what is actually
fragile small frameworks, although at some locations they observed. On one hand its location favours capturing dense
build dense decimetre-sized clusters. They preferentially shelf water formed in the gulfs of Roses and Lion to the
develop on the most abrupt parts of the canyon walls, and north (Canals et al. 2006; Ribó et al. 2011), which enhances
the largest colonies occur in protected overhangs, which downcanyon flows and food arrival favouring CWC develop-
represent the locations less exposed to sedimentation and ment, even though water temperature is generally slightly
impacts from commercial trawling. Colonies are most beyond the species optimal conditions. Measurements in
common along the first kilometre of the eastern wall of July 2011 at the exact locations where corals develop in Cap
Cap de Begur branch, and on the opposite western wall de Begur branch reveal bottom temperatures from 13.3 to
28 A Cold-Water Coral Habitat in La Fonera Submarine Canyon 293
13.5 °C, and salinities from 38.18 to 38.36. On the other Acknowledgements This research was supported by the European
Union’s DG Environment programme through research project IDEM
hand, coastline closeness can also involve an excess of sedi- (Implementation of the MSFD to the DEep Mediterranean Sea,
ment arrival during eastern storms (Martín et al. 2006), when agreement number 11.0661/2017/750680/SUB/ENV.C2), the Spanish
the wave base attains larger depths over the shelf thus easing project ROV-CAÑONES (CTM2009-06778-E), a Catalan Government
the transport of resuspended sediments into the canyon. This Grups de Recerca Consolidats grant (2017 SGR 315), and the French
Agence Nationale de la Recherche contract SunRISE (ANR-
would be particularly relevant in Illa Negra and Sant Sebastià 14-
CE01-0016). We thank people involved in sea going activities,
branches, while the Cap de Begur branch, and also the more reviewers V.A.I. Huvenne and J. Rivera, as well as editor C. Orejas for
distant sections of Illa Negra branch where corals grow, their comments.
would be more protected from this increase in sediment
arrival while still benefiting from such highly energetic
processes.
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both the geographic spread and the depth range of the CWC
habitat and their forming species in the Mediterranean Sea.
The research work summarised here also addresses directly
one of the main future challenges in submarine canyon Cross References
research highlighted in Canals et al. (2013), which is the
nature of the links between high-energy oceanographic Aymà A, Aguzzi J, Canals M, et al (this volume) Occurrence of living
processes and the deep ecosystem, as well as the subsequent northwestern Mediterranean sea
action-response effects between such processes and deep Fourt M, Goujard A, Chevaldonné P (this volume) Working with visual
ecosystem biodiversity and biological processes at both spe- methods, comparison among the French deep-sea canyons
cies and community levels. Puig P, Gili JM (this volume) Submarine canyons in the Mediterranean:
a shelter for cold-water corals
Cold-Water Coral Associated Fauna
in the Mediterranean Sea and Adjacent 29
Areas
José L. Rueda, Javier Urra, Ricardo Aguilar,

Lorenzo Angeletti, Marzia Bo, Cristina García-Ruiz,
Manuel M. González-Duarte, Eduardo López,
Teresa Madurell, Manuel Maldonado, Ángel Mateo-
Ramírez, César Megina, Juan Moreira, Francina Moya,
Lais V. Ramalho, Antonietta Rosso, Cèlia Sitjà,
and Marco Taviani
Abstract (ca. 50 spp.), fishes (ca. 50 spp.), echinoderms (ca. 20

Cold-water corals are recognised as a key component of spp.) and brachiopods (7 spp.). Most species are not uni-
Mediterranean deep-sea ecosystems but the knowledge of vocally linked to cold-water corals, but they benefit from
their associated biodiversity is still limited. To date, the the complex and diverse microhabitats provided by them.
fauna associated to the Central Mediterranean cold-water There is a clear need to continue the investigation of
coral habitats is the best known (e.g. the cold-water coral Mediterranean cold-water coral habitats to fully docu-
provinces of Santa Maria di Leuca, Bari canyon and Strait ment the faunistic inventory, biogeographic connections
of Sicily) but such knowledge should be extended to the and functions of the many species connected to such
whole Mediterranean Basin. The combined biodiversity emblematic ecoystems of the deep-sea.
censed so far for Mediterranean cold-water coral habitats
and those of adjacent areas (Strait of Gibraltar-Gulf of
Cádiz) includes a conspicuous number of species (ca. 520 Keywords
spp.) with a high representation of sponges (ca. 90 spp.), Biodiversity · Cold-water coral · Benthic community ·
polychaetes (ca. 90 spp.), cnidarians (ca. 80 spp.), bryo- Demersal fauna · Mediterranean Sea
zoans (ca. 75 spp.), crustaceans (ca. 60 spp.), molluscs
J. L. Rueda (*) · C. García-Ruiz · F. Moya

Centro Oceanográfico de Málaga, Instituto Español de
M. M. González-Duarte · C. Megina
Oceanografía, Málaga, Spain
Departamento de Zoología, Facultad de Biología, Universidad de
Sevilla, Sevilla, Spain
J. Urra
E. López · J. Moreira
Centro Oceanográfico de Málaga, Instituto Español de
Departamento de Biología, Universidad Autónoma de Madrid,
Oceanografía, Málaga, Spain
Madrid, Spain
Departamento de Biología Animal, Universidad de Málaga,
T. Madurell
Málaga, Spain
Institut de Ciències del Mar (ICM-CSIC),
R. Aguilar Barcelona, Catalonia, Spain
Fundación Oceana, Madrid, Spain
M. Maldonado · C. Sitjà
L. Angeletti Center for Advanced Studies of Blanes (CEAB-CSIC),
Institute of Marine Sciences (ISMAR-CNR), Bologna, Italy Girona, Spain
M. Bo Á. Mateo-Ramírez
Dipartimento di Scienze della Terra, dell’Ambiente e della Vita, Departamento de Biología Animal, Universidad de Málaga,
Università degli Studi di Genova, Genova, Italy Málaga, Spain

https://doi.org/10.1007/978-3-319-91608-8_29
296 J. L. Rueda et al.
29.1 H
istorical Background on Cold-Water losa and the cemented bivalve Spondylus gussonii, as well
Coral Associated Fauna as the serpulid polychaete Metavermilia multicristata.
in the Mediterranean These authors pointed out that most CWC in the
Mediterranean were represented by dead subfossil findings,
The scientific attention on cold-water coral (CWC) grounds is overall representing a low diversity assemblage with
steadily increasing worldwide leading to a better definition of respect to Atlantic counterparts. Thus, it was postulated
such fundamental deep-sea habitats (hereafter CWC habitats) that Atlantic-type CWC flourished in the Mediterranean
at regional and global scales, with respect to their biodiversity, basin during the Pleistocene and then their prosperity
ecological role, functioning and ecosystem services (Roberts declined drastically. This concept got direct support by
et al. 2006). The demanding study of the benthic, suprabenthic extensive dating showing that, in fact, most CWC samples
and demersal biota taking advantage of such CWC habitats are late Pleistocene in age (Delibrias and Taviani 1984;
requires resources and time, with results, therefore, appearing Malinverno et al. 2010; McCulloch et al. 2010; Taviani
only years after the discovery of these habitats. The et al., this volume; Vertino et al., this volume). Moreover,
Mediterranean is not an exception, and this explains why only associated fauna to such Pleistocene CWC were also iden-
limited, albeit growing, information is at present available on tified, mainly represented by scleractinians (Zibrowius
its CWC sites. Admitedly, most of the living CWC sites of the 1980) and molluscs that included the large limid Acesta
Mediterranean and adjacent areas have only been detected excavata and gastropods (Taviani and Colantoni 1979;
since the year 2000 onwards, with the likely expectation that Taviani and Taviani 1986).
more will be tracked in the future (Fig. 29.1). A revolution in the knowledge of CWC habitats then took
Early observations on the presence of CWC in the place due to the discovery of extensive live coral grounds
Mediterranean Sea are accidental, mainly referring to with L. pertusa and M. oculata off Cape Santa Maria di
Madrepora oculata, and based upon sea-cable recovery and Leuca (SML) in the northern Ionian Sea between 300 and
fisheries, especially as by-catch of invasive tecnhiques for 1100 m depth (Mastrototaro et al. 2002; Tursi et al. 2004;
harvesting red coral (Zibrowius 1980, 2003). In the past, Taviani et al. 2005). This CWC province houses a diverse
the occasional occurrence of CWC like M. oculata and community of associated organisms (Mastrototaro et al.
Lophelia pertusa was reported from various Mediterranean 2010; Rosso et al. 2010; D’Onghia et al. 2011; D’Onghia,
locations (Zibrowius 1980), although generally deprived of this volume; Chimienti et al., this volume) and still represents
information on its accompanying associated biota. A first the best case-study for the Mediterranean Sea in terms of
turning point for the comprehensive appreciation of research devoted to its various aspects such as habitat char-
Mediterranean CWC must be credited to Pérès and Picard acterisation and mapping (Vertino et al. 2010; Savini et al.
(1964) who described the CWC associated community as 2014; Angeletti et al., this volume; Lo Iacono et al., this vol-
Biocoenose des “coraux blancs” (White-coral biocoeno- ume), the diverging hard and soft-bottom thanatofacies
sis). Their study benefited from the pre-existing research (Rosso et al. 2010), assessment of its benthic and demersal
carried out on Atlantic CWC associated fauna, from the fauna (Tursi et al. 2004; Mastrototaro et al. 2010; Vertino
experience gained through deep-sea dredging and trawling, et al. 2010), taxonomical aspects of specific benthic groups
as well as from the submergible surveys at different loca- (e.g. sponges, meiofauna, molluscs) (Longo et al. 2005;
tions specifically in the Mediterranean Sea. Pérès and Bongiorni et al. 2010; Negri and Corselli 2016 respectively),
Picard (1964) detected some species which were later con- the megafauna and commercial resources (D’Onghia et al.
sistently found to be associated with CWC in the 2010, 2011; D’Onghia, this volume) and the evaluation of
Mediterranean basin, such as the byssate Asperarca nodu- the trophic web (Carlier et al. 2009).
L. V. Ramalho M. Taviani
Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Institute of Marine Sciences (ISMAR-CNR), Bologna, Italy
Rio de Janeiro, RJ, Brazil
A. Rosso Woods Hole, MA, USA
Dipartimento di Scienze Biologiche, Geologiche e Ambientali,
Università degli Studi di Catania, Catania, Italy
CoNISMa – Consorzio Nazionale Interuniversitario per le Scienze
del Mare, Rome, Italy
29 Cold-Water Coral Associated Fauna in the Mediterranean Sea and Adjacent Areas 297
Fig. 29.1 Main areas with studies on associated fauna of cold-water Capo Spartivento canyons; Urania Bank (69); Dohrn canyon (24);
coral habitats in the Mediterranean Sea and adjacent areas. Codes for Malta escarpment (4, 24); Santa Maria di Leuca (18, 19, 20, 35, 40, 43,
references in Table 29.1: Gazul mud volcano (16, 46, 53, 54); Strait of 52, 66); Off Tricase (3, 61); Bari canyon (3, 21, 57, 61); Off Montenegro
Gibraltar (2); Guadiaro canyon (65); Djibouti bank (27, 32, 45); Chella (3, 61); Kephalonian Ridge (42); Crete, Karpathos and Rhodes margins
bank (1, 13, 34, 45); Cabliers bank (45, 55); Cap de Creus canyon (28, (Taviani et al. 2011b)
38, 44, 68); Lacaze-Duthiers canyon (22); Var canyon (22); Nora and
Further deep-sea exploration quickly detected CWCs in mented CWC in the southern Adriatic whose megabenthic
other areas of the Central Mediterranean, demonstrating that fauna share many traits with the SML coral province
the SML coral province was not the only one in the (Freiwald et al. 2009; Angeletti et al. 2014; Taviani et al.
Mediterranean (Freiwald et al. 2009). Some of these CWC 2016).
sites were located on bedrock overhangs on steeply inclined In other sectors of the Mediterranean Sea and adjacent
submarine walls and escarpments that are difficult to sample, areas (Strait of Gibraltar, Gulf of Cádiz) the knowledge on
and most of the associated fauna is still to be characterised in the CWC associated fauna is not as detailed as for SML. In
the coming years (Schembri et al. 2007; Angeletti et al. the eastern Mediterranean, there is a scarce occurrence of
2015). In some seafloor structures of the Central CWC habitats (some of them dominated by living
Mediterranean (e.g. Bari Canyon in the southwestern Desmophyllum dianthus and Dendrophyllia ramea, the latter
Adriatic Sea), general studies on habitats and associated observed off Cyprus at 125–170 m depth by Orejas et al.
macro and megafauna communities documented the pres- 2017a, this volume), and studies on the associated mega-
ence of living colonies of M. oculata (together with fauna have only been carried out off the south western coasts
Leiopathes glaberrima, small colonies of L. pertusa and of Kephalonia Island (Greece) (Mytilineou et al. 2014),
clusters of Dendrophyllia cornigera), and some of the asso- along the margins of Crete, Karpathos and Rhodes as well as
ciated species (especially serpulids, sponges, bryozoans and in the Sea of Marmara (Taviani et al. 2011b) and off Cyprus
fishes) were then documented (Sanfilippo et al. 2013; (Jiménez et al. 2016). In the western Mediterranean, recent
D’Onghia et al. 2015; D’Onghia, this volume). In the Strait findings of CWC were obtained using ROV in the Capo
of Sicily (SoS) various CWC sites were detected (Zibrowius Spartivento canyon system, including the Nora canyon
and Taviani 2005; Schembri et al. 2007; Freiwald et al. 2009) (South Sardinia CWC province) (Taviani et al. 2017), which
and their associated macrofauna is getting increasing atten- has filled a gap not only in the known CWC geographic dis-
tion for its richness (Schembri et al. 2007; Mifsud et al. tribution within the Mediterranean Sea but also on the asso-
2009; Taviani et al. 2009, 2010, 2011b; Deidun et al. 2015). ciated CWC fauna for western Mediterranean locations
Remotely operated vehicle (ROV) surveys have also docu- (Taviani et al. 2017). Further north, shallow buried subfossil
deep-coral mounds were located in the Tuscan Archipielago, 29.2 E

cological Role of Mediterranean CWC
and their dominant sessile macrofauna described (Remia and Habitats for the Associated Fauna
Taviani 2005). Recent unpublished information confirms the
occurrence of live M. oculata in this area (Taviani, pers. Mediterranean CWC habitats are functionally and morpho-
comm.). The Catalan-Provençal-Ligurian submarine can- logically complex deep-sea habitats that form an intricate
yons also represent an important Mediterranean area with network of biogenic frames and interstices, providing niches,
CWC habitats (Domínguez-Carrió et al. 2014), however spawning, nursery or shelter ground for a large variety of
CWC studies have only dealt with the habitat-forming spe- organisms, including commercially important and threat-
cies (Orejas et al. 2009; Gori et al. 2013; Lastras et al. 2016, ened species (Table 29.1). Unlike the NE Atlantic, studies
this volume; Aymà et al., this volume; Fourt et al., this vol- evaluating the ecological role of Mediterranean CWC habi-
ume; Puig and Gili, this volume), the fish community (de tats for the associated fauna are still scarce as commented on
Lucia et al. 2008) or the megabenthic fauna, which only rep- the previous section.
resent a small fraction of the associated biodiversity Primarily, CWC habitats provide a suitable substrate both
(Madurell et al. 2012b; Fabri et al. 2014, 2017; Fanelli et al. for larval settlement and adult growth, adding to the number
2017). Nevertheless, the only study on the planktonic com- of hard substrates in the deep-sea which are scarcer than the
munity of Mediterranean CWC habitats was performed in prevailing soft bottoms (Zibrowius 2003). These habitats
one of these canyons (Cap de Creus) (Madurell et al. 2012a). also increase the hard bottom complexity providing
In the western Mediterranean, dense coral forests of the tridimensional structure and offering a complex network of
bamboo coral Isidella elongata have been discovered in the biogenic interstices for many species in comparison to other
last decade, some of them apparently displaying very well- types of hard and soft bottoms (Tursi et al. 2004; Longo et al.
developed communities (Cartes et al. 2013; Bo et al. 2015; 2005; Mastrototaro et al. 2017). As detected in the NE
Mastrototaro et al. 2017; Pierdomenico et al. 2018). In the Atlantic, the complexity of the CWC habitat in some
Alborán Sea, important CWC habitats have also been Mediterranean areas (e.g. SML) is enhanced by other sessile
detected (Wienberg and Titschack 2017; Lo Iacono et al., species that develop on coral skeletons, such as sponges or
this volume) and some studies have partially characterised polychaetes (e.g. serpulids, Eunice norvegica), that also
the associated megabenthic community in the Chella (Seco create a complex living tridimensional structure for species
de los Olivos) and Cabliers banks (Pardo et al. 2011; of different taxa (Longo et al. 2005; Mastrototaro et al. 2010;
Sánchez-Gallego et al. 2014; de la Torriente et al. 2014), Mueller et al. 2013). Bongiorni et al. (2010) detected higher
Djibouti banks (Hebbeln et al. 2009; Pardo et al. 2011), meiofaunal diversity due to the effects on habitat
Melilla coral province (Hebbeln et al. 2009; Lo Iacono et al. heterogeneity/complexity in both living coral and coral
2014, this volume) and Guadiaro canyon (Vázquez et al. rubble of SML than in surrounding slope sediments,
2016). However, detailed studies on the biodiversity are still concluding that the protection of dead corals, a so-far almost
missing for any of the CWC habitats of the Alborán Sea neglected habitat in terms of biological conservation, can
which represents an important area, together with the Gulf of further contribute to the maintenance of a high deep-sea
Cádiz (GoC), to better understand the distributional patterns biodiversity along continental margins (Henry and Roberts
of the associated fauna between the Mediterranean Sea and 2007; Rossi et al. 2017). The presence of soft bottoms in
the Atlantic Ocean. This is also the case for the Strait of areas with coral rubble among live CWC colonies may also
Gibraltar, where CWC habitats have also been detected and favor the occurrence of typical bathyal soft bottom fauna
their scleractinian species identified, but no studies on other within the CWC habitats. Indeed, these areas with mixed
components of their associated fauna have ever been done bottoms can display a high biodiversity due to the higher
(Álvarez-Pérez et al. 2005). microhabitat complexity (Rosso et al. 2010; Vertino et al.
In the GoC, impinged by the Mediterranean Outflow 2010). The comparisons at SML between different types of
Water current (MOW), there is a widespread occurrence of CWC related habitats, that were sampled with similar
last glacial assemblages containing CWC (Taviani et al. methods, disclosed a lower biodiversity for living coral
1991; Wienberg et al. 2009). Interestingly, extensive live colonies of Madrepora oculata and Lophelia pertusa (30
CWC habitats have been detected during the last years in taxa), than for dead coral branches (83 taxa) and for coral
specific areas of the GoC (e.g. Gazul mud volcano), rubble (59 taxa) (Mastrototaro et al. 2010). The authors
representing benthic and demersal biodiversity hotspots for indicated that this is probably due to the use of the exposed
the GoC (Díaz del Rio et al. 2014; Rueda et al. 2016; Orejas dead coral skeleton as attachment sites for a great number of
et al. 2017b). sessile invertebrates because of the antifouling properties of
the coral coenosarc or due to the instability of this living
tissue (Jensen and Frederiksen 1992; Mortensen and Fosså
Table 29.1 Faunistic list of organisms found inhabiting cold-water CWC), dominant (D; species in high numbers at least at some studied
coral (CWC) ecosystems and surrounding habitats in the Mediterranean locations), common (C; species frequently observed in some studied
Sea and Gulf of Cádiz, indicating whether they are strict (S; species locations, although not strictly abundant) or occasional (O; species
displaying a strong relationship with CWC and predominantly found in cited occasionally in any studied location)
Species S D C O Habitats Locations References

PORIFERA Demospongiae
Acantheurypon pilosella (Topsent, 1904) + Mo, Lp, Dd CS 62
Alectona millari Carter, 1879 + Mo, Lp, Dd CS 62
Anisocrella hymedesmina Topsent, 1927 + M-coral-R CCa, GoC 46, 64
Antho signata (Topsent, 1904) + Mo, Lp, Dd SML 35, 40
Antho involvens (Schmidt, 1864) + Mo BCa 21
Axinella cannabina (Esper, 1794) + Mo, Lp, Dd SML 35, 40
Axinella pumila Babiç, 1922 + Mo BCa 21
Biemna partenopea Pulitzer-Finali, 1978 + Mo BCa 21
Biemna tenuisigma Pulitzer-Finali, 1978 + Mo BCa 21
Bubaris carcisis Vacelet, 1969 + M-coral-R SCa 64
Bubaris subtyla Pulitzer-Finali, 1983 + Mo BCa 21
Bubaris vermiculata (Bowerbank, 1866) + Mo, M-coral-R BCa, CCa 21, 64
Calthropella pathologica (Schmidt, + Mo, Lp, Dd, M-coral-R SML, CCa 35, 40, 64
1868)
Characella pachastrelloides (Carter, + Lp, coral-R Malta, GMV, GoC 10, 16
1876)
Chelonaplysilla psammophila (Topsent, + M-coral-R CCa 64
1928)
Clathria anchorata (Carter, 1874) + Mo, Lp, Dd, M-coral-R CS, CCa 62, 64
Clathria frogeti (Vacelet, 1969) + M-coral-R CCa 64
Clathria gradalis Topsent, 1925 + Mo BCa 21
Cliona sp. + Mo, Lp SML 35, 40
Crella alba (Vacelet, 1969) + M-coral-R CCa 64
Crellastrina alecto (Topsent, 1898) + Mo, Lp, Dd SML 35, 40
Damiria curvata (Vacelet, 1969) + M-coral-R CCa 64
Dercitus plicatus (Schmidt, 1868) + Mo, Lp SML 40
Desmacella annexa Schmidt, 1870 + Mo, Lp, Dd SML 35, 40
Desmacella inornata (Bowerbank, 1866) + Mo, Lp, Dd, M-coral-R SML, BCa, CCa, CS, GMV 35, 40, 46, 21, 62,
64
Dragmatella aberrans (Topsent, 1890) + M-coral-R CCa 64
Erylus discophorus (Schmidt, 1862) + Lp Malta 10
Erylus papulifer Pulitzer-Finali, 1983 + Mo, Lp, Dd SML 35, 40
Esperiopsis strongylophora Vacelet, 1969 + M-coral-R CCa 64
Eurypon clavatum (Bowerbank, 1866) + Mo, Lp SML 40
Eurypon cinctum Sarà, 1960 + Mo BCa 21
Eurypon denisae Vacelet, 1969 + M-coral-R CCa 64
Eurypon hispidulum (Topsent, 1904) + M-coral-R CCa 64
Eurypon obtusum Vacelet, 1969 + M-coral-R SCa 64
Eurypon topsenti Pulitzer-Finali, 1983 + Mo BCa 21
Eurypon viride (Topsent, 1889) + Mo BCa 21
Geodia nodastrella Carter, 1876 + Mo, Lp, Dd SML 35, 40
Geodia anceps (Vosmaer, 1894) + Mo, Lp, Dd SML 35, 40
Haliclona arnesenae (Arndt, 1927) + M-coral-R CCa 64
Haliclona magna (Vacelet, 1969) + M-coral-R CCa 64
Haliclona mucosa (Griessinger, 1971) + Mo, Lp GMV 54
Hamacantha azorica Topsent, 1904 + Lp Lis, GMV 10, 16
Hamacantha falcula (Bowerbank, 1874) + Mo, Lp, Dd, M-coral-R CS, BSL 62, 64
Hamacantha johnsoni (Bowerbank, + Mo, Lp, Dd, M-coral-R SML, BCa, CCa, CS 35, 40, 21, 62, 64
1864)
Hamacantha lundbecki Topsent, 1904 + M-coral-R CCa 64
Hamacantha papillata Vosmaer, 1885 + Mo, Lp, Dd, M-coral-R SML, BCa, PCa 35, 40, 21, 64
(continued)
Hexadella cf. cripta Reveillaud, + Mo CCa 23
Allewaert, Pérez, Vacelet, Banaigs &
Vanreusel, 2012
Hexadella dedritifera Topsent, 1913 + Mo, Lp, Dd SML 35, 40
Hexadella pruvoti Topsent, 1896 + Mo BCa 21
Hymedesmia gracilisigma Topsent, 1928 + M-coral-R CCa 64
Hymedesmia inflata Vacelet, 1969 + M-coral-R CCa 64
Hymedesmia plicata Topsent, 1928 + M-coral-R PCa 64
Hymedesmia pugio Lundbeck, 1910 + coral-R Lis, GMV 10, 16
Hymedesmia mutabilis (Topsent, 1904) + Mo, Lp, Dd, M-coral-R SML, CS, CCa 35, 40, 62, 64
Hymedesmia serrulata Vacelet, 1969 + M-coral-R CCa 64
Hymerhabdia oxytrunca Topsent, 1904 + Mo, M-coral-R BCa, CCa 21, 64
Hymerhabdia typica Topsent, 1892 + Mo BCa 21
Janulum spinispiculum (Carter, 1876) + Lp, M-coral-R Lis, GMV, CCa 10, 16, 64
Jaspis incrustans (Topsent, 1890) + Mo, Lp SML, LIs, BCa, GMV 35, 40, 10, 16, 21
Latrunculia rugosa (Vacelet, 1969) + M-coral-R CCa 64
Leiodermatium cf. lynceus Schmidt, 1870 + Mo, Lp SML 35, 40
Lycopodina hypogea (Vacelet & + Mo, Dc, Dd ChBa, Urania bank, LIs 1
Boury-Esnault, 1996)
Melonanchora emphysema (Schmidt, + M-coral-R CCa 64
1875)
Pachastrella monilifera Schmidt, 1868 + Mo, Lp SML, BCa, CS 35, 40, 21, 62
Penares euastrum (Schmidt, 1868) + coral-R GoC 46
Petrosia sp. + Mo GMV 54
Phakellia robusta Bowerbank, 1866 + Mo, Lp LIs, BCa, GMV 10, 16, 21
Plocamionida ambigua (Bowerbank, + Mo, Lp, Dd SML 35, 40
1866)
Poecillastra compressa (Bowerbank, + Mo, Lp, M-coral-R SML, BSL, Magaud bank, 35, 40, 21, 62, 64,
1866) BCa, CS, GoC, CCCa 17
Podospongia lovenii Barboza du Bocage, + M-coral-R BSL, CCa 64
1869
Polymastia polytylota Vacelet, 1969 + M-coral-R BSL 64
Prosuberites longispinus Topsent, 1893 + Mo BCa 21
Pseudotrachya hystrix (Topsent, 1890) + M-coral-R CCa 64
Rhabdeurypon spinosum Vacelet, 1969 + M-coral-R CCa 64
Rhizaxinella pyrifera (Delle Chiaje, + M-coral-R EM, Cca, Corsica 32, 64
1828)
Sceptrella insignis (Topsent, 1890) + Mo, Lp, Dd, M-coral-R SML, BCa, CCa, CS 35, 40, 21, 62, 64
Siphonidium ramosum (Schmidt, 1870) + Mo, Lp, Dd SML 35, 40
Siphonodictyon infestum (Johnson, 1889) + Mo SML, BCa 6, 2
Spiroxya levispira (Topsent, 1898) + Mo, Lp, Dd SML, CS 35, 6, 40, 62
Spiroxya heteroclita Topsent, 1896 + Mo, Lp, Dd SML 35, 40
Stelligera rigida (Montagu, 1814) + M-coral-R CCa 64
Stylocordyla pellita (Topsent, 1904) + M-coral-R Cerigotto channel 64
Suberites sp. 1 + Mo, Lp SML 40
Suberites sp. 2 + Mo, Lp SML 40
Sulcastrella tenens (Vacelet, 1969) + M-coral-R CCa 64
Thrombus abyssi (Carter, 1873) + Mo, Lp, Dd, coral-R SML, GoC 35, 40
Timea chondrilloides (Topsent, 1904) + Mo, Lp, Dd, M-coral-R SML, CCa 35, 40, 64
Vulcanella gracilis (Sollas, 1888) + Mo, Lp, coral-R, LIs, Malta, SML, CS, CCa 35, 40, 10, 62, 64
M-coral-R
PORIFERA Hexactinellida
Asconema setubalense Kent, 1870 + Mo, Lp DBa, GMV 45, 16
Farrea sp. + Mo CCa 23
Nodastrella nodastrella (Topsent, 1915) + coral-R DBa 32
Oopsacas minuta Topsent, 1927 + Mo CCa 23
(continued)
Sympagella delauzei Boury-Esnault, Vacelet, Reiswig + Mo, Lp, coral-R ChBa 13
& Chevaldonné, 2015
Tretodictyum cf. tubulosum Schulze, 1886 + Mo CCa 23
PORIFERA Homoscleromorpha
Plakina monolopha Schulze, 1880 + Mo, Lp SML 40
Plakortis simplex Schulze, 1880 + Mo, Lp, Dd SML, BCa 35, 40, 21
CNIDARIA Hydrozoa
Acryptolaria conferta (Allman, 1877) + Mo, Lp, coral-R SML, GdC, SoG, AS 37, 40, 47, 46
Acryptolaria crassicaulis (Allman, 1888) + Mo, Lp, coral-R GMV 46
Aglaophenia tubulifera (Hincks, 1861) + coral-R SoG 47
Antennella secundaria (Gmelin, 1791) + Mo, Lp, coral-R SoG, GdC 47, 46
Bedotella armata (Pictet & Bedot, 1900) + Mo, Lp GMV 46
Campanularia hincksii Alder, 1856 + Mo, Lp, coral-R GMV 46
Cladocarpus sinuosus Vervoort, 1966 + Mo, Lp GMV 46
Clytia gracilis (Sars, 1850) + coral-R GMV 46
Clytia linearis (Thornely, 1900) + Mo, Lp SML 40
Cryptolaria pectinata (Allman, 1888) + Mo, Lp, coral-R SoG, GdC 47, 46
Diphasia margareta (Hassall, 1841) + Mo, Lp GMV 16
Halecium labrosum Alder, 1859 + Mo, Lp SML 40
Halopteris catharina (Johnston, 1833) + coral-R SoG 47
Hybocodon cf. prolifer Agassiz, 1860 + Mo, Lp SML 40
Lafoea dumosa (Fleming, 1820) + coral-R GdC 47
Laodicea undulata (Forber & Goodsir, + Mo, Lp SML 40
1853)
Lytocarpia myriophyllum (Linnaeus, + coral-R GMV 46
1758)
Mitrocoma annae Haeckel, 1864 + Mo, Lp SML 40
Modeeria rotunda (Quoy & Gaimard, + coral-R GMV 46
1827)
Nemertesia antennina (Linnaeus, 1758) + Mo, Lp SML, GdC 40, 46
Nemertesia falcicula Ramil & Vervoort, + Mo, Lp GMV 46
1992
Nemertesia ramosa (Lamarck, 1816) + Mo, Lp SML 40
Polyplumaria flabellata Sars, 1874 + Mo, Lp, coral-R GdC, GMV 37, 16
Racemoramus panicula (G.O. Sars, + coral-R GdC, GMV 47, 46
1874)
Schizotricha frutescens (Ellis & Solander, + Mo, Cr, Cs, Dc FCa 33
1786)
Sertularella gayi (Lamouroux, 1821) + Mo, Cr, Cs, Dc, coral-R GdC, GMV, FCa 33, 47, 46
Streptocaulus cf. pectiniferus Allman, + coral-R GMV 46
1883
Tubiclavoides striatum Moura, Cunha & + Mo, Lp GdC 41
Schuchert, 2007
Turritopsis cf. nutricula McCrady, 1857 + coral-R GMV 46
Zygophylax biarmata Billard, 1905 + Mo, Lp, coral-R GdC, SoG 37, 47, 46
Zygophylax cf. brownei Billard, 1924 + Mo, Lp GMV 46
CNIDARIA Anthozoa, Hexacorallia
Amphianthus dohrnii (Koch, 1878) + Mo, Lp SML, EM 40, 66, 32
Antipathella subpinnata (Ellis & + RBB GoL, GMV 22, 16
Solander, 1786)
Antipathes dichotoma Pallas, 1766 + coral-R, RBB DBa, SML, GoL, CCa 66, 45, 22, 24
Caryophyllia calveri Duncan, 1873 + Mo, Lp, RBB SML 40, 66, 52
Caryophyllia cyathus (Ellis & Solander, + coral-R, RBB SoG 2
1786)
Caryophyllia inornata (Duncan, 1878) + coral-R, RBB SoG 2
Caryophyllia smithii Stokes & Broderip, + coral-R GMV 16
1828
(continued)
Dendrophyllia cornigera (Lamarck, + Mo, Lp, coral-R, RBB DBa, CaBa, ChBa, SML, SAS, 2, 24, 44, 66, 52,
1816) SoG, GoL, GMV, CCCa, Malta, 45, 28, 16, 3, 22,
BCa, EM, FCa 33, 17, 18, 32
Desmophyllum dianthus (Esper, 1794) + Mo, Lp, RBB NBa, SML, BCa, CCa, SAS, 2, 69, 58, 24, 40,
SoG, GoL, EM, CaBa, ChBa, 52, 66 45, 8, 3, 22,
CCCa 62, 32, 17
Edwardsiella loveni (Carlgren, 1892) + Mo, Lp, coral-R LigurianSea, NBa, DBa 50, 69, 32
Eguchipsammia gaditana (Duncan, 1873) + Mo, coral-R GMV 16
Epizoanthus sp. + Mo, Lp SML 40, 66
Flabellum chunii Marenzeller, 1904 + coral-R GMV 16
Isozoanthus primnoidus Carreiro-Silva, Braga- + Cv, Sv, lithistids NWSicily, NBa, GoL 66, 9, 21
Henriques, Sampaio, de Matos, Porteiro & Ocaña,
2010
Kadophellia bathyalis Tur, 1991 + coral-R, RBB SML, SAS 40, 52, 3
Leiopathes glaberrima (Esper, 1788) + Mo, Lp, RBB, coral-R CaBa, DBa, SML, SAS, GoL, 66, 45, 3, 22, 16,
GMV 32
Lophelia pertusa (Linnaeus, 1758) + Lp, Mo, coral-R, RBB DBa, ChBa, CaBa, SML, GMV, 2, 24, 44, 66, 52,
SoG, SoS, GoL, CS, FCa, 45, 28, 4, 22, 33,
CCCa, Malta, BCa, SAS, NBa, 17, 18, 62, 32, 16,
EM 3
Madrepora oculata Linnaeus, 1758 + Lp, Mo, coral-R, RBB DBa, ChBa, CaBa, SML, GMV, 2, 24, 44, 66, 52,
SoS, GoL, CS, FCa, CCCa, 45, 28, 22, 33, 17,
NBa, Malta, BCa, SAS, Gca, 18, 62, 65, 32, 16,
EM, SoG 3, 4
Parantipathes larix (Esper, 1788) + coral-R, RBB CaBa, EM 45, 3
Parazoanthus anguicomus (Norman, + Spongesamongcoral-R BCa 8
1868)
Peachia cylindrica (Reid, 1848) + SB SML, BCa 40, 3
Protanthea simplex Carlgren, 1891 + coral-R NBa 69
Sagartia elegans (Dalyell, 1848) + Mo, Lp SML 40, 66
Sagartia troglodytes (Price in Johnston, + Mo, Lp SML 40, 66
1847)
Stenocyathus vermiformis (Pourtalès, + Mo, Lp, RBB SML, SoS, SAS, SoG, NBa 2, 69, 24, 40, 52,
1868) 66, 3
Thalamophyllia gasti (Döderlein, 1913) + RBB NBa 69
CNIDARIA Anthozoa, Octocorallia
Acanthogorgia armata Verrill, 1878 + coral-R, RBB CaBa 45
Acanthogorgia hirsuta Gray, 1857 + coral-R, RBB, Mo SAS, SML, CaBa, GMV, EM, 63, 40, 3, 45, 16,
CCa 32, 24
Anthomastus sp. + RBB CaBa 45
Bebryce mollis Philippi, 1842 + coral-R, RBB SML 40, 66, 3
Callogorgia verticillata (Pallas, 1766) + coral-R, RBB, Mo SAS, SML, DBa, CaBa, GoL, 63, 45, 3, 22, 24
CCa
Cavernularia pusilla (Philippi, 1835) + coral-R AS 45
Corallium rubrum (Linnaeus, 1758) + Mo, Lp, RBB NBa, GoL, FCa 69, 11, 22, 33, 18
Dendrobrachia bonsai Lopez-Gonzales + Mo, Lp SML, NBa 40, 69
& Cunha, 2010
Eunicella cavolini (Koch, 1887) + Mo, Lp, RBB GoL 22
Eunicella verrucosa (Pallas, 1766) + RBB CaBa, ChBa 45
Funiculina quadrangularis (Pallas, 1766) + SB DBa, ChBa 52, 45, 22
Isidella elongata (Esper, 1788) + SB DBa, CaBa, ChBa, SML, SoS, 69, 24, 40, 66, 52,
NBa 45
Kophobelemnon stelliferum (Müller, + SB DBa, CaBa, ChBa 45
1776)
Paramuricea clavata (Risso, 1826) + Mo, Lp, RBB GoL, ChBa 45, 22
Paramuricea macrospina (Koch, 1882) + coral-R, RBB SML, SAS 40, 66, 3
Pennatula phosphorea Linnaeus, 1758 + coral-R AS 45
(continued)
Placogorgia spp. + Mo, Lp GMV 16
Scleranthelia rugosa var. musiva Studer, + coral-R NBa 69
1878
Plexauridae spp. + Mo CCa 24
Swiftia pallida Madsen, 1970 + coral-R, RBB SML 40
Swiftia rosea (Grieg, 1887) + RBB CaBa 45
Viminella flagellum (Johnson, 1863) + Mo, coral-R GMV, CCa 16, 24
ANNELIDA Polychaeta
Aglaophamus cf. elamellatus (Eliason, + M-coral-R GoC 12
1951)
Ampharetidae + M-coral-R GoC 12
Aricidea cf. pseudoarticulata Hobson, + M-coral-R GoC 12
1972
Aricidea simonae Laubier & Ramos, + M-coral-R GoC 12
1974
Bathyvermilia eliasoni (Zibrowius, 1970) + Mo, Lp, M-coral-R SML, BCa 63, 40, 57, 16
Bispira sp. + BM BCa 3
Bonellia sp. + BM BCa 24
Bonellia viridis Rolando, 1822 + BM, coral-R CS, EM 62, 3
Capitellidae + M-coral-R GoC 12
Cirratulidae + M-coral-R GoC 12
Dodecaceria sp. + M-coral-R GoC 12
Eclysippe sp. + M-coral-R GoC 12
Eunice dubitata Fauchald, 1974 + M-coral-R GoC 12
Eunice norvegica (Linnaeus, 1767) + + Mo, Lp, Pm, M-coral-R, SML, Malta, GMV, BCa 63, 58, 12, 40, 66,
BM 57, 16, 21, 62
Eunice sp. + BM GoC 67
Exogone sp. + M-coral-R GoC 12
Fauveliopsis sp. + M-coral-R GoC 12
Filograna implexa Berkeley, 1835 + + Mo, Lp, Pm, M-coral-R, SML, BCa 63, 40, 21
BM
Filograna sp. + + Mo, Lp, Dc, Pm, NBa, Messina Strait, BCa, 68, 7, 57, 16, 21,
M-coral-R, Ant GMV 69
Filogranula annulata (O.G. Costa, 1861) + Mo SML 56
Filogranula gracilis Langerhans, 1884 + + Mo, Lp, Dc, M-coral-R, SML, NBa, BCa 63, 68, 40, 57, 16,
BM 21, 69
Filogranula stellata (Southward, 1963) + + Mo, Lp, M-coral-R SML, GoC 63, 40, 67
Flabelligeridae + M-coral-R GoC 12
Galathowenia oculata (Zachs, 1923) + M-coral-R GoC 12
Glycera tesselata Grube, 1840 + M-coral-R GoC 12
Goniadidae + M-coral-R GoC 12
Haplosyllis chamaeleon Laubier, 1960 + + Pc Chafarinas Islands 36
Haplosyllis spongicola (Grube, 1855) + M-coral-R GoC 12
Harmothoe cf. evei Kirkegaard, 1980 + M-coral-R GoC 12
Harmothoe vesiculosa Ditlevsen, 1917 + Mo, Lp SML 40
Helmutneris flabellicola (Fage, 1936) + Fc GMV 16
Hesionidae + M-coral-R SML 40
Hyalopomatus madreporae Sanfilippo, + + + Mo, Lp, Dc, Pm, BM SML, BCa 56, 40, 57, 21
2009
Hyalopomatus variorugosus Ben-Eliahu + + Mo, M-coral-R NBa, SML 68, 56
& Fiege, 1996
Janita fimbriata (Delle Chiaje, 1822) + M-coral-R, BM NBa, SML, BCa 68, 69, 40, 21
Lanice conchilega (Pallas, 1766) + BM Cabliers Bank, GoC, FCa 45, 67, 33
Leiochrides sp. + M-coral-R SML 40
Leitoscoloplos mammosus Mackie, 1987 + M-coral-R GoC 12
Leocrates atlanticus (McIntosh, 1885) + M-coral-R GoC, SML 12, 40
(continued)
Lumbrineriopsis paradoxa (Saint-Joseph, + M-coral-R GoC 12
1888)
Lumbrineris latreilli Audouin & Milne + M-coral-R SML 40
Edwards, 1834
Lumbrineris sp. + M-coral-R SML 40
Lysidice ninetta Audouin & H Milne + M-coral-R GoC 12
Edwards, 1833
Lysippe cf. fragilis (Wollebaek, 1912) + M-coral-R GoC 12
Magelona wilsoni Glémarec, 1966 + M-coral-R GoC 12
Maldanidae + M-coral-R GoC 12
Metavermilia multicristata (Philippi, + Mo, Lp, Dc, M-coral-R, SML, NBa, BCa 63, 68, 40, 57, 21,
1844) BM 69
Nephtys cf. paradoxa Malm, 1874 + M-coral-R SML 40
Nothria conchylega (Sars, 1835) + M-coral-R SML 40
Notomastus sp. + M-coral-R GoC 12
Oweniidae + M-coral-R SML 40
Paradiopatra hispanica (Amoureux, + M-coral-R GoC 12
1972)
Paraonidae + M-coral-R GoC 12
Parasabella sp. + Encrusted calcareous BCa 3
sediments
Pareurythoe borealis (M. Sars, 1862) + M-coral-R GoC 12
Phalacostemma sp. + M-coral-R GoC,SML 12, 40
Pholoe sp. + M-coral-R SML 40
Pholoides dorsipapillatus (Marenzeller, + M-coral-R GoC 12
1893)
Phyllodoce cf. maculata (Linnaeus, + M-coral-R GoC 12
1767)
Phyllodoce madeirensis Langerhans, + M-coral-R GoC 12
1880
Phyllodoce mucosa Örsted, 1843 + M-coral-R SML 40
Pionosyllis nidrosiensis (Bidenkap, 1907) + M-coral-R GoC 12
Placostegus tridentatus (Fabricius, 1779) + + M-coral-R, BM NBa, BCa 68, 69, 21
Poecilochaetus sp. + M-coral-R GoC 12
Prionospio sp. + M-coral-R GoC 12
Protula sp. + M-coral-R NBa 68, 69
Protula tubularia (Montagu, 1803) + Mo, Dc FCa 33
Sabella pavonina Savigny, 1822 + Mo, Dc FCa 33
Sabellidae + M-coral-R GoC 12
Salmacina dysteri (Huxley, 1855) + + Mo, Dc FCa 33
Scolelepis sp. + M-coral-R GoC 12
Semivermilia agglutinata (Marenzeller, + M-coral-R NBa 68, 69
1893)
Serpula concharum Langerhans, 1880 + BM BCa 21
Serpula vermicularis Linnaeus, 1767 + + Mo, Lp, Dc, Dd, SML, NBa, BCa, CS 63, 68, 40, 3, 57,
M-coral-R, BM 21, 62, 69
Serpulidae + BM GoC 67
Siboglinum sp. + M-coral-R GoC 12
Sigalionidae + M-coral-R GoC 12
Sphaerosyllis cf. pirifera Claparède, 1868 + M-coral-R GoC 12
Spiochaetopterus sp. + M-coral-R GoC 12
Spiophanes sp. + M-coral-R GoC 12
Subadyte pellucida (Ehlers, 1864) + Mo, Lp, M-coral-R GoC, SML 12, 40
Synelmis sp. + M-coral-R GoC 12
Terebellidae + M-coral-R SML 40
Vermiliopsis monodiscus Zibrowius, 1968 + + Mo, Lp, Dc, M-coral-R, NBa, SML, BCa 68, 40, 57, 21
BM
(continued)
Vermiliopsis sp. + Mo, Dc, M-coral-R NBa, SAS, FCa 68, 3, 33, 69
SIPUNCULA Sipunculidea
Golfingiidae + M-coral-R GoC 12
SIPUNCULA Phascolosomatidea
Apionsoma murinae bilobatae (Cutler, + M-coral-R SML 40
1969)
Aspidosiphon muelleri muelleri Diesing, + M-coral-R SML 40
1851
MOLLUSCA Gastropoda
Alvania cimicoides (Forbes, 1844) + coral-R SML 52
Alvania testae (Aradas & Maggiore, 1844) + coral-R SML 43
Anatoma tenuis (Jeffreys, 1877) + Mo, Lp, coral-R SML 52
Anekes sculpturata Warén, 1992 + coral-R DBa 27
Babelomurex sentix Bayer, 1971 + Mo, Lp, Dd, Cr Malta 60
Callostracon thyrrenicum (Smriglio & + coral-R SML 43
Mariottini, 1996)
Cirsonella romettensis (Granata-Grillo, + coral-R DBa 27
1877)
Coralliophila richardi (P. Fischer, 1882) + Mo, Lp Malta 60
Coralliophila squamosa (Bivona Ant. in + Mo, Lp Tuscan archip., NBa, GMV 60, 16
Bivona And., 1838)
Danilia tinei (Calcara, 1839) + coral-R SML, GMV 54, 16, 43
Emarginula adriatica (O.G. Costa, 1829) + Mo, Lp SML, GMV 63, 54, 43
Emarginula multistriata Jeffreys, 1882 + Mo, Lp, coral-R SML, GMV 54, 16, 27, 43
Emarginula tenera Locard, 1892 + Mo, Lp, coral-R SML 43
Epitonium algerianum (Weinkauff, 1866) + Mo, Lp, coral-R GMV 54, 16
Epitonium celesti (Aradas, 1854) + Mo, Lp, coral-R GMV 54, 16
Fusinus rostratus (Olivi, 1792) + coral-R SML 43
Iphitus tuberatus Jeffreys, 1883 + Dc Alboran Island, off Granada 39, 27
Lissotesta turrita (Gaglini, 1987) + Mo, Lp, coral-R ChBa 27
Mitrella pallaryi (Dautzenberg, 1927) + Mo, Lp, coral-R GMV 54, 16
Mathilda cochlaeformis Brugnone, 1873 + coral-R SML 43
Nassarius lima (Dillwyn, 1817) + coral-R SML 52, 43
Pagodula echinata (Kiener, 1840) + coral-R SML 52
Pleurotomella demosia (Dautz & Fischer, + coral-R SML 43
1896)
Putzeysia wiseri (Calcara, 1842) + coral-R SML 52, 43
Solatisonax bannocki (Melone & Taviani, + coral-R SML 43
1980)
MOLLUSCA Bivalvia
Abra longicallus (Scacchi, 1835) + coral-R SML 52
Acesta excavata (Fabricius, 1779) + Mo, Lp Dohrn canyon Angeletti (comm.
pers.)
Asperarca nodulosa (Müller, 1776) + Mo, Lp, HB, coral-R SML, GMV 63, 40, 52, 54, 16,
43
Astarte sulcata (da Costa, 1778) + coral-R GMV 54, 16
Bathyarca philippiana (Nyst, 1848) + Mo, Lp, coral-R SML, GMV 63, 54, 43
Coralliophaga lithophagella (Lamarck, + Mo, Lp, coral-R GMV 16
1819)
Cyclopecten hoskynsi (Forbes, 1844) + coral-R SML 52
Delectopecten vitreus (Gmelin, 1791) + Mo, Lp SML, BCa 63, 21, 43
Ennucula aegeensis (Forbes, 1844) + coral-R SML 52, 43
Rocellaria dubia (Pennant, 1777) + Mo, Lp, coral-R GMV 16
Heteranomia squamula (Linnaeus, 1758) + Mo, Lp, coral-R SML 52, 43
Hiatella arctica (Linnaeus, 1767) + coral-R SML 43
Karnecampia sulcata (Müller, 1776) + coral-R SML 43
Kelliella miliaris (Philippi, 1844) + coral-R SML 52
(continued)
Ledella messanensis (Jeffreys, 1870) + coral-R SML 52
Lima marioni Fischer, 1882 + Mo, Lp, coral-R GMV 54, 16
Limopsis aurita (Brocchi, 1814) + coral-R GMV 16
Limea crassa (Forbes, 1844) + coral-R SML 52
Neopycnodonte cochlear (Poli, 1795) + Mo, Lp Lacaze-Duthier 22
Neopycnodonte zibrowii Gofas, Salas & + Mo, Lp Sicilian channel 24
Taviani, 2009
Heteranomia squamula (Linnaeus, 1758) + Mo, Lp, coral-R SML 52
Spondylus gussonii (O.G. Costa, 1829) + Mo, Lp SML, Cassidaigne, GMV 63, 22, 27, 49, 43
Yoldiella lucida (Lovén, 1846) + coral-R SML 52
MOLLUSCA Scaphopoda
Antalis agilis (M. Sars in G.O. Sars, + coral-R SML 52
1872)
MOLLUSCA Cephalopoda
Onychoteuthis banksii (Leach, 1817) + Mo, Lp, HB SML 19
Pteroctopus tetracirrhus (Delle Chiaje, + Mo, Lp, HB SML 19
1830)
Todarodes sagittatus (Lamarck, 1798) + Mo, Lp BCa 21
CRUSTACEA Amphipoda
Amphipoda + Mo CCCa 38
Harpinia dellavallei Chevreux, 1910 + Mo CCCa 38
Iphimedia obesa Rathke, 1843 + Mo CCCa 38
Melphidippella macra (Norman, 1869) + Mo CCCa 38
Normanion ruffoi Diviacco & Vader, + Mo CCCa 38
1988
Paraphoxus oculatus (G. O. Sars, 1879) + Mo CCCa 38
Perrierella audouiniana (Bate, 1857) + Mo CCCa 38
Platyscelus ovoides (Risso, 1816) + Mo CCCa 38
Primno sp. + Mo CCCa 38
Vibilia armata Bovallius, 1887 + Mo CCCa 38
CRUSTACEA Cirripedia
Megabalanus tulipiformis (Ellis, 1758) + Mo, Lp Sardinia, Sicily 48
Metaverruca recta (Aurivillius, 1898) + Mo, Lp SML 15
Pachylasma giganteum (Philippi, 1836) + Mo, Lp, coral-R Messina Strait, Malta 48, 58
Scalpellum scalpellum (Linnaeus, 1767) + Mo, Lp SML 15
CRUSTACEA Copepoda
Acartia sp. + Mo CCCa 38
Calanus helgolandicus (Claus, 1863) + Mo CCCa 38
Calanoida + Mo CCCa 38
Centropages sp. + Mo CCCa 38
Diaixis pygmaea (Scott T., 1894) + Mo CCCa 38
Harparcticoida + Mo CCCa 38
Oithonak sp. + Mo CCCa 38
Pleuromamma sp. + Mo CCCa 38
CRUSTACEA Decapoda
Acanthephyra eximia Smith, 1884 + Mo, Lp SML 63
Anamathia rissoana (Roux, 1828) + Mo, Lp, Dd SML, Malta, CS 58, 40, 62
Aristaeomorpha foliacea (Risso, 1827) + Mo, Lp SML 63
Aristeus antennatus (Risso, 1816) + Mo, Lp SML 63, 19
Bathynectes maravigna (Prestandrea, + Mo, Lp, coral-R SML, DBa, EM 63, 3
1839)
Ebalia nux A. Milne-Edwards, 1883 + coral-R SML 52
Ebalia sp. + Mo, Lp, Dd CS 62
Geryon longipes A. Milne-Edwards, 1882 + Mo, Lp SML 40
Homola barbata (Fabricius, 1793) + Mo, Lp, Dd CS 62
(continued)
Inachus leptochirus Leach, 1817 + Mo, Lp, HB GMV 16
Jaxea nocturna Nardo, 1847 + Mo CCCa 38
Macropipus tuberculatus (Roux, 1830) + Mo, Lp SML 40
Monodaeus couchii (Couch, 1851) + Mo, Lp SML, GMV 63, 16
Munida intermedia A. Milne Edwards & + Mo, Lp SML, GMV 63, 16
Bouvier, 1899
Munida sp. + Mo, coral-R ChBa, CCCa 45, 38
Munida tenuimana Sars, 1872 + Mo, Lp SML, CS 40, 62
Paguridae + Mo, Lp SML, CCCa 40, 38
Palinurus mauritanicus Gruvel, 1911 + Mo, Lp DBa, EM 45, 3
Paromola cuvieri (Risso, 1816) + Mo, Lp, Dd BCa, CS 21, 62
Philocheras bispinosus (Hailstone, 1835) + Mo CCCa 38
Plesionika acanthonotus (Smith, 1882) + Mo, Lp SML 63
Plesionika cf. gigliolii (Senna, 1902) + Mo, Lp, Dd CS 62
Plesionika heterocarpus(A. Costa, 1871) + Mo, Lp SAS 61
Plesionika martia (A. Milne-Edwards, + Mo, Lp, coral-R SML 40, 19
1883)
Plesionika sp. + Mo, Lp, Dd CS 62
Polycheles typhlops Heller, 1862 + Mo, Lp SML 40
Scyllarus arctus (Linnaeus, 1758) + Mo, Lp AS 45
CRUSTACEA Euphausiacea
Euphasiacea Mo, Lp, Dd CS 62
Nyctiphanes couchii (Bell, 1853) + Mo CCCa 38
Stylocheiron suhmi G.O. Sars, 1883 + Mo, Lp SML 40
CRUSTACEA Isopoda
Gnathia sp. + Mo CCCa 38
CRUSTACEA Mysidacea
Anchialina agilis (G.O. Sars, 1877) + Mo CCCa 38
Leptomysis gracilis (G.O. Sars, 1864) + Mo CCCa 38
Lophogaster typicus Sars, 1857 + Mo CCCa 38
Siriella sp. + Mo CCCa 38
CRUSTACEA Ostracoda
Bairdoppilata conformis (Terquem, + Mo, Lp, coral-R SML 59
1878)
Bythocypris obtusata (Sars, 1866) + Mo, Lp, coral-R SML 59
ECHINODERMATA Echinoidea
Brissopsis atlantica mediterranea + Mo, Lp SML 40
Mortensen, 1913
Cidaris cidaris (Linnaeus, 1758) + Mo, Lp, Ant, Dc, Dd, Cr SAS, BCa, SML, Malta, CS, 63, 58, 40, 66, 45,
GoL, DBa, CaBa, ChBa, GMV, 3, 13, 22, 55, 33,
EM 18, 54, 62, 32
Echinus melo Lamarck, 1816 + + Mo, Lp, Dd, Dc, Cr BCa, SML, CS, GoL, FCa, 40, 3, 13, 22, 33,
ChBa, DBa 62, 32
Gracilechinus acutus (Lamarck, 1816) + + Mo, Lp, Dd, Dc, Cr BCa, SML, GoL, FCa, ChBa, 40, 13, 22, 21, 33,
GMV 54, 18
ECHINODERMATA Holothuroidea
Holothuria forskali Delle Chiaje, 1823 + Mo, Dc, Cr, Dd FCa, ChBa 13, 33
Holothuria tubulosa Gmelin, 1791 + Mo, Lp, Dd ChBa 13
Mesothuria intestinalis (Ascanius, 1805) + Mo, Lp SML 40
Parastichopus regalis (Cuvier, 1817) + Mo, Lp, Dd SML, ChBa 63, 40, 13
Psolidium complanatum Cherbonnier, + Mo, Lp, Dd NBa 68
1969
ECHINODERMATA Ophiuroidea
Amphiura filiformis (O.F. Müller, 1776) + Mo, Lp BCa, SML 63, 40, 21
Astrospartus mediterraneus (Risso, 1826) + Mo, Dc, Cr GoL, FCa 22, 33
Ophiothrix fragilis (Abildgaard in + Mo, Lp, Dd ChBa, EM 13, 3
O.F. Müller, 1789)
(continued)
Ophiothrix quinquemaculata (Delle + Mo BCa 21
Chiaje, 1828)
Ophiothrix sp. + Mo, Lp, Dc, Cr FCa, GMV, GCa 33, 54, 65
ECHINODERMATA Asteroidea
Chaetaster longipes (Retzius, 1805) + Mo, Lp GMV 16
Hacelia superba H.L. Clark, 1921 + Mo, Lp, Dc GMV 53, 54
Odontaster mediterraneus (Marenzeller, + Mo, Lp SML 40, 66
1893)
Odontaster sp. + Mo, Lp, Ant, Dc SAS 3
Peltaster placenta (Müller & Troschel, + Mo, Lp, Ant, Cv, Dc, Dd BCa, Malta, CS 3, 14, 62
1842)
ECHINODERMATA Crinoidea
Leptometra phalangium (Müller, 1841) + Mo, Lp, Ant NWSicily, DBa, CaBa, GMV 45, 9, 16, 55
BRYOZOA Gymnolaemata
Aetea sica (Couch, 1844) + Mo SML 40
Aetea truncata (Landsborough, 1852) + Mo BCa 21
Amphiblestrum ruggeroi Rosso, 1999 + Mo, Lp CM 68
Buskea dichotoma (Hincks, 1862) + Mo CM 68
Callopora dumerilii (Audouin, 1826) + Mo, Lp CM 68
Cellaria salicornioides Lamouroux, 1816 + Mo, Lp CM 68
Copidozoum exiguum (Barroso, 1920) + Mo, Lp CM, IonianSea, SML, SoS 29, 68, 51, 40, 52
Copidozoum tenuirostre (Hincks, 1880) + Lp CM 68
Copidozoum planum (Hincks, 1880) + Dd WM 26
Copidozoum balgimae Reverter-Gil & + Mo AS 28
Fernandez-Pulpeiro, 1999
Coronellina fagei Gautier, 1962 + Mo SoS 29
Crassimarginatella crassimarginata + Mo CM, WM 68, 26
(Hincks, 1880)
Crepis harmelini Reverter-Gil, Souto & + Mo, Lp SoG 29
Fernández-Pulpeiro, 2011
Distansescharella alcicornis (Jullien, + Mo, Lp SoG 31
1882)
Escharella acuta Zabala, Maluquer & + Lp CM 68
Harmelin, 1993
Escharella longicollis (Jullien, 1882) + Mo, Lp SoG 31
Escharella octodentata (Hincks, 1880) + Lp CM 68
Escharella ventricosa (Hassal, 1842) + Mo, Dc WM, SML 25, 26
Escharina dutertrei protecta Zabala, + Mo, Lp, Dc CM, WM, Toulon 23, 24, 65
Maluquer & Harmelin, 1993
Escharina vulgaris (Moll, 1803) + Mo, Lp CM, BCa 68, 2
Fenestrulina malusii (Audouin, 1826) + Mo, Lp CM 68
Gregarinidra gregaria (Heller, 1867) + Mo, Lp CM, BCa, WM 26, 68, 21
Haplopoma sciaphilum Silén & + Mo SoS 29
Harmelin, 1976
Herentia hyndmanni (Johnston, 1847) + Mo, Lp, Dc CM, SML, BCa, WM, SoS 25, 26, 29, 68, 5,
40, 52, 21
Hincksina longispinosa Harmelin & + Mo SoG 30
d’Hondt, 1992a
Hippomenella mucronelliformis (Waters, + Mo BCa 21
1899)
Hippothoa flagellum Manzoni, 1870 + Mo, Lp CM 68
Mollia patellaria (Moll, 1803) + Mo WM 26
Myriapora truncata (Pallas, 1766) + Mo, Lp BCa 24
Neolagenipora eximia (Hincks, 1860) + Mo, Lp CM 68
Onychocella marioni (Jullien, 1882) + Mo WM 26
Palmiskenea gautieri Madurell, Zabala, + Dc WM 24
Domínguez-Carrió & Gili, 2013
(continued)
Palmiskenea skenei (Ellis & Solander, + Lp CM 68
1786)
Porella minuta (Norman, 1868) + Mo WM 26
Cribrilaria hincksii (Friedl, 1917) + Lp CM 68
Cribrilaria innominata (Couch, 1844) + Mo CM 68
Cribrilaria radiata (Moll, 1803) + Mo, Lp CM, BCa 68, 2
Cribrilaria pseudoradiata Harmelin & + Mo SML 40
Aristegui, 1988
Cribrilaria venusta (Canu & Bassler, + Mo, Dc BCa, WM, SML 21, 25, 26
1925)
Puellina setosa (Waters, 1899) + Mo SoS 29
Puellina scripta (Reuss, 1848) + Mo, Lp, Ca AS 31
Glabrilaria pedunculata (Gautier, 1956) + Mo, Dc BCa, Toulon, SoS, SML 25, 29, 40, 21
Reteporella sparteli (Calvet, 1906) + Mo, Lp SML 52
Schizomavella cf. discoidea (Busk, 1859) + Mo BCa 21
Schizomavella fischeri (Jullien, 1882) + Mo, Lp SML 40, 5
Schizomavella linearis (Hassall, 1841) + Mo, Lp, Dc CM, BCa 68, 2
Schizomavella neptuni (Jullien, 1882) + Mo, Lp CM, SML, SoS 29, 68, 40, 52
Schizoretepora longisetae + Dc WM 26
(Canu & Bassler, 1928)
Scrupocellaria delilii (Audouin, 1826) + Mo, coral-R CM, BCa, SML, CS 68, 52, 21, 62
Scrupocellaria incurvata Waters, 1896 + Mo, Dc CM, WM, SML 25, 26, 68
Setosella cavernicola Harmelin, 1978 + Mo SoS 29
Setosella vulnerata (Busk, 1860) + Mo, Lp CM, SML 68, 40
Smittina cervicornis (Pallas, 1766) + Mo, Lp, Dc SAS, BCa 57, 62
Smittina crystallina (Norman, 1867) + Mo, Lp CM, BCa, SML, IonianSea 68, 51, 40, 52, 21
Smittoidea ophidiana (Waters, 1879) + Mo, Lp CM, BCa 68, 2
Smittoidea reticulata (MacGillivray, + Mo, Lp CM 68
1842)
Stephanollona armata (Hincks, 1862) + Mo WM 26
Stephanotheca arrogata (Waters, 1879) + Mo SoS, BCa, WM 26, 2
Stephanotheca watersi Reverter-Gil, Souto & + Mo BCa 20
Fernández-Pulpeiro, 2012
Tessaradoma boreale (Busk, 1860) + Mo, Lp SML 40, 52
Teuchopora edwardsi (Jullien, 1882) + Mo, Lp SoG 31
Turbicellepora coronopus (Wood, 1844) + Mo, Lp CM, BCa 68, 2
BRYOZOA Stenolaemata
Anguisia verrucosa Jullien, 1882 + Mo SML 40
Crisia ramosa Harmer, 1891 + Mo BCa 21
Crisia sigmoidea (Waters, 1916) + Mo CM 68
Crisia tenella Calvet, 1906 + Mo SML, BCa 40, 52, 21
Entalophoroecia deflexa (Couch, 1844) + Mo, Lp CM, BCa, SoS 29, 68, 21
Entalophoroecia robusta Harmelin, 1976 + Lp CM 68
Exidmonea coerulea (Harmelin, 1976) + Lp CM 68
Exidmonea flexuosa (Pourtalès, 1867) + Mo, Lp SoG 31
Plagioecia patina (Lamarck, 1816) + Mo, Lp CM 68
Plagioecia inoedificata (Jullien, 1882) + Mo SoS 29
Stomatopora gingrina Jullien, 1882 + Mo CM, SoS 29, 68
Tervia barrieri Rosso, 1998 + Mo, Lp SML 52
BRACHIOPODA Rhynchonellata
Gryphus vitreus (Born, 1778) + Mo, Lp, coral-R, Lp, NBa, SML, CS, CCCa, ChBa, 34, 68, 40, 38, 16,
Dd, HB DBa, GMV 17, 62, 32
Megathiris detruncata (Gmelin, 1791) + coral-R, HB NBa, ChBa 34, 68
Megerlia truncata (Linnaeus, 1767) + Mo, Lp, coral-R, HB NBa, SML, CS, CCCa, ChBa 34, 68, 40, 1, 38,
62, 17
Platidia sp. + coral-R NBa 68
Terebratulina retusa (Linnaeus, 1758) + coral-R, HB CS, ChBa 34, 1, 62
(continued)
BRACHIOPODA Craniata
Novocrania anomala (O. F. Müller, 1776) + Mo, Lp, coral-R, HB SAS, CS, ChBa, GMV 34, 3, 16, 62
Novocrania sp. + coral-R NBa 68
FISH Actinopteri
Acantholabrus palloni (Risso, 1810) + Mo CS 62
Arctozenus risso (Bonaparte, 1840) + Mo, Lp SML, DBa 19, 3
Aulopus filamentosus (Bloch, 1792) + Mo, Lp SML 19
Bathypterois dubius Vaillant, 1888 + Mo, Lp SML 63
Benthocometes robustus (Goode and + Mo, Lp SML, CS 63, 19, 62
Bean, 1886)
Brama brama (Bonnaterre, 1788) + Mo, Lp SML 18, 20
Capros aper (Linnaeus, 1758) + M-coral-R EM 32
Chlorophthalmus agassizi Bonaparte, + Mo, Lp SML, CS 19, 62
1840
Coelorinchus caelorhincus (Risso, 1810) + Mo, Lp SML, CaBa, CS, EM 63, 19, 45, 62, 32
Conger conger (Linnaeus, 1758) + Mo, Lp, Ant SML, CaBa, CIs 63, 18, 19, 20, 45,
42
Coryphaena hippurus Linnaeus, 1758 + Mo, Lp SML 18
Epigonus constanciae (Giglioli, 1880) + Mo CS 62
Gadella maraldi (Risso, 1810) + Mo, coral-R GMV 16
Helicolenus dactylopterus (Delaroche, + Mo, Lp, Ant SML, CaBa, CIs, Malta, CS, 63, 18, 19, 20, 45,
1809) GMV, EM 42, 4, 62, 16, 32
Hoplostethus mediterraneus Cuvier, 1829 + Mo, Lp SML, CaBa 63, 45
Hymenocephalus italicus Giglioli, 1884 + Mo, Lp SML 63, 19
Lepidion lepidion (Risso, 1810) + Mo, Lp SML 63, 19
Lepidopus caudatus (Euphrasen, 1788) + Mo, Lp, Ant SML, Malta, CS, GMV 18, 19, 20, 4, 62,
16
Lepidorhombus whiffiagonis (Walbaum, + Mo CS 62
1792)
Macroramphosus scolopax (Linnaeus, + Ant Malta 4
1758)
Merluccius merluccius (Linnaeus, 1758) + Mo, Lp, Ant SML, CIs 18, 19, 20, 42
Micromesistius poutassou (Risso, 1826) + Mo, Lp, Ant SML, CaBa, DBa, CIs, GMV 18, 20, 45, 42, 16
Molva dipterygia (Pennant, 1784) + Mo, Lp SML 18, 20
Mora moro (Risso, 1810) + Mo, Lp, Ant SML, CIs 63, 18, 19, 20, 42
Nettastoma melanurum Rafinesque, 1810 + Mo, Lp SML 19
Nezumia aequalis (Günther, 1878) + Ie GMV 16
Nezumia sclerorhynchus (Valenciennes, + Mo, Lp SML 63, 19
1838)
Notacanthus bonaparte Risso, 1840 + Mo, Lp SML 63, 19
Pagellus bogaraveo (Brünnich, 1768) + Mo, Lp SML, CaBa, ChBa, CS, EM 18, 19, 20, 45, 62,
32
Phycis blennoides (Brünnich, 1768) + Mo, Lp, Ant SML, CIs, CS, GMV, EM 63, 18, 19, 20, 42,
62, 16, 32
Polyprion americanus (Bloch and + Mo, Lp, Ant SML, Malta, CS, DBa 20, 4, 62, 32
Schneider, 1801)
Ruvettus pretiosus Cocco, 1833 + Mo, Lp SML 18
Scorpaena elongata Cadenat, 1943 + Mo CS 62
Scorpaena scrofa Linnaeus, 1758 + Mo, Lp Dba, CaBa 45
Sudis hyalina Rafinesque, 1810 + Mo, Lp SML 19
FISH Elasmobranchii
Centrophorus granulosus (Bloch and + Mo, Lp SML 18, 20
Schneider, 1801)
Chimaera monstrosa Linnaeus, 1758 + Mo, Lp SML 63, 19
Dalatias licha (Bonnaterre, 1788) + Mo, Lp SML, CaBa 63, 45
Dipturus oxyrinchus (Linnaeus, 1758) + Mo, Lp SML 63, 18, 20
(continued)
Etmopterus spinax (Linnaeus, 1758) + Mo, Lp SML 63, 18, 19, 20
Galeus melastomus Rafinesque, 1810 + Mo, Lp SML, GMV, ChBa 63, 18, 19, 20, 16,
13
Hexanchus griseus (Bonnaterre, 1788) + Mo, Lp SML 18
Leucoraja circularis (Couch, 1838) + Mo, Lp SML 18, 20
Leucoraja fullonica (Linnaeus, 1758) + Mo, Lp SML 20
Prionace glauca (Linnaeus, 1758) + Mo, Lp SML 20
Pteroplatytrygon violacea (Bonaparte, + Mo, Lp SML 20
1832)
Scyliorhinus canicula (Linnaeus, 1758) + M-coral-R EM 32
Squalus blainville (Risso, 1827) + Ant CIs 42
Codes for habitat-forming species and bottom types: Mo Madrepora oculata, Lp Lophelia pertusa, Dd Desmophyllum dianthus, Dc Dendrophyllia
cornigera, Cr Corallium rubrum, Cs Caryophyllia smithii, Ca Caryophyllia cyathus, Fc Flabellum chunii, Cv Callogorgia verticillata, Lg
Leiopathes glaberrima, Ie Isidella elongata, Sv Stenocyathus vermiformis, Pc Paramuricea clavata, Ant Anthipatarian banks, Pm Pachastrella
monilifera, SB soft bottoms, HB hard bottoms, RBB rocky benches and boulders, BM bathyal mud, coral-R coral rubble, M-coral-R mud mixed
with coral-R
Codes for locations: SoG Strait of Gibraltar, SoS Strait of Sicily, GoC Gulf of Cadiz, GoL Gulf of Lion, WM western Mediterranean, AS Alboran
Sea, SAS South Adriatic Sea, CM Catalan margin, CS Capo Spartivento, SML Santa Maria di Leuca, BCa Bari canyon, FCa La Fonera canyon,
CCCa Cap de Creus canyon, GCa Guadiaro canyon, CCa Cassidaigne canyon, SCa Sicié canyon, PCa Planier canyon, CaBa Cabliers bank, DBa
Djinouti bank, ChBa Chella bank, NBa Nameless bank, LIs, Linosa island, CIs, Kephalonia island, GMV Gazul mud volcano, EM East Melilla
Codes for references: 1. Aguilar et al. (2011), 2. Álvarez-Pérez et al. (2005), 3. Angeletti et al. (2014), 4. Angeletti et al. (2015), 5. Berning et al.
(2008), 6. Beuck et al. (2010), 7. Bo et al. (2009), 8. Bo et al. (2012), 9. Bo et al. (2014), 10. Calcinai et al. (2013), 11. Costantini et al. (2010), 12.
Da Silva (2009), 13. de la Torriente et al. (2014), 14. Deidun et al. (2015), 15. Di Geronimo (2010), 16. Díaz del Rio et al. (2014), 17. Domínguez-
Carrió et al. (2014), 18. D’Onghia et al. (2010), 19. D’Onghia et al. (2011), 20. D’Onghia et al. (2012), 21. D’Onghia et al. (2015), 22. Fabri et al.
(2014), 23. Fabri et al. (2017), 24. Angeletti, Taviani pers. obs., 25. Gautier (1958), 26. Gautier (1962), 27. Gofas et al. (2011), 28. Gori et al.
(2013), 29. Harmelin (1979), 30. Harmelin and d’Hondt (1992a), 31. Harmelin and d’Hondt (1992b), 32. Hebbeln et al. (2009), 33. Lastras et al.
(2016), 34. Llompart (1988), 35. Longo et al. (2005), 36. López et al. (1996), 37. López-González and Cunha (2010), 38. Madurell et al. (2012b),
39. Margelli et al. (1995), 40. Mastrototaro et al. (2010), 41. Moura et al. (2007), 42. Mytilineou et al. (2014), 43. Negri and Corselli (2016), 44.
Orejas et al. (2009), 45. Pardo et al. (2011), 46. present study (INDEMARES/CHICA project), 47. Ramil and Vervoort (1992), 48. Relini (1980),
49. Remia and Taviani (2005), 50. Rossi (1958), 51. Rosso (2003), 52. Rosso et al. (2010), 53. Rueda et al. (2011), 54. Rueda et al. (2016), 55.
Sánchez-Gallego et al. (2014), 56. Sanfilippo (2009), 57. Sanfilippo et al. (2013), 58. Schembri et al. (2007), 59. Sciuto and Rosso (2015), 60.
Taviani et al. (2009), 61. Taviani et al. (2016), 62. Taviani et al. (2017), 63. Tursi et al. (2004), 64. Vacelet (1969), 65. Vázquez et al. (2016), 66.
Vertino et al. (2010), 67. Wienberg et al. (2009), 68. Zabala et al. (1993), 69. Zibrowius and Taviani (2005)
2006). In the western Mediterranean, Maynou and Cartes both Atlantic and Mediterranean CWC habitats for some
(2012) observed that areas with large stands of Isidella elon- commercial species, such as Helicolenus dactylopterus
gata support higher species richness, abundance and bio- which feeds on benthic crustaceans, fishes as well as plank-
mass of crustaceans compared to close muddy bottoms tonic organisms that generally occur in these habitats
where Isidella was not present. These communities present (Mortensen 2000; D’Onghia et al. 2012). Specific food
an overall high invertebrate diversity, with a faunal sources of CWC habitats are CWC themselves, which are
assemblage comprising about 170 invertebrate taxa and 61 consumed by gastropods that are strictly associated with
species of fish (Mastrototaro et al. 2017). CWC (e.g. Muricidae-Coralliophilinae, Nystiellidae,
The CWC habitats generally provide a wide diversity of Epitoniidae) (Taviani et al. 2009).
food sources due to the increased local biodiversity, as a The CWC habitats may provide an important spawning,
result of the habitat complexity, and the large and wide nursery and/or shelter area for mobile species from adjacent
variety of species that benefit from that (Mastrototaro et al. habitats (D’Onghia et al. 2010, 2012; Maynou and Cartes
2010, 2017). In general, sediments in areas occupied by 2012; Mastrototaro et al. 2017; Chimienti et al., this volume;
CWCs display higher quantity and greater nutritional quality D’Onghia, this volume). Some species may occur at higher
of organic matter (Bongiorni et al. 2010). Moreover, CWC densities (Pagellus bogaraveo, Conger conger, H.
habitats frequently occur in areas with high hydrodynamic dactylopterus) or display larger sizes (Galeus melastomus,
conditions and food supply that favor the presence of other Etmopterus spinax, C. conger, H. dactylopterus) in
sessile suspensivores (e.g. sponges, gorgonians, black corals) Mediterranean CWC habitats in comparison to adjacent
(e.g. Domínguez-Carrió et al. 2014; Rueda et al. 2016). An bottoms (D’Onghia et al. 2012). Regarding invertebrate
increase of prey diversity and density is suggested to occur in commercial species, Maynou and Cartes (2012) observed
that some of them were more abundant or reached larger 1992; Vertino et al. 2014, this volume). As documented for
sizes in areas with high densitiy of I. elongata, particularly Atlantic CWC habitats, important components of the
the red shrimp Aristeus antennatus and Plesionika martia. Mediterranean CWC associated fauna seem to also include
Nevertheless, it is difficult to demonstrate whether these spe- sponges, molluscs, bryozoans and cnidarians (Jensen and
cies are less abundant in adjacent sedimentary habitats due to Frederiksen 1992; Mastrototaro et al. 2010; Chimienti et al.,
the fishing effects rather than more abundant in CWC habi- this volume). Some of the common and dominant associated
tats due to the increased habitat complexity and prey abun- taxa are similar in both basins (e.g. Eunice norvegica,
dance and diversity (D’Onghia et al. 2012; Mastrototaro Coralliophila richardi, Asperarca nodulosa, Delectopecten
et al. 2017). Regarding this, D’Onghia et al. (2010) indicated vitreus, Heteranomia squamula, etc.), but some of the typical
that future research must address the importance of CWC associated species in Atlantic CWC habitats are generally
habitats as an “essential fish habitat” (EFH) for creating absent or uncommon in Mediterranean ones (Jensen and
“Deep-sea Fisheries Restricted Areas” (FRA) as imple- Frederiksen 1992; Tursi et al. 2004; López-Correa et al. 2005;
mented by the General Fisheries Commission for the Mortensen and Fosså 2006; Mastrototaro et al. 2010).
Mediterranean (GFCM) (see also D’Onghia, this volume). Nevertheless, recent surveys using ROV are providing new
data on Atlantic species occurring on Mediterranean CWC
habitats (Mastrototaro et al. 2017). One of the typical compo-
29.3 S
patial Differentiation of the CWC nents on Atlantic CWC habitats is the bivalve Acesta excav-
Associated Fauna in the Atlanto- ata which seems to be very rare in CWC habitats of the
Mediterranean Context Mediterranean Sea and the GoC (López-Correa et al. 2005).
This mollusc is the largest known bivalve associated with
Studies on fauna associated with CWC have been done in CWC and was widespread throughout the Mediterranean Sea
different areas of the Mediterranean Sea and at different during the last glacial period, and live-individuals still occur
bathymetric ranges. Nevertheless, due to the difficulty of in different parts of the western Mediterranean, for instance in
sampling CWC habitats, different methodological the Var and Dohrn canyons (North Tyrrhenian Sea) (López-
approaches were used and this creates difficulties when Correa et al. 2005) (Fig. 29.2).
comparing spatial and bathymetric patterns of the CWC As reported for the Atlantic banks (Jensen and Frederiksen
associated fauna. A high biodiversity has been found in 1992; Mortensen and Fosså 2006), there is generally not a
CWC habitats of SML in comparison to other Mediterranean specific fauna associated with CWC habitats (Mastrototaro
locations. This is surely the result of extensive multi-gear et al. 2010). In agreement with Roberts et al. (2009), species
sampling and the collaboration of experts working on recorded within or around CWC banks are drawn from the
different taxonomic groups, therefore biodiversity regional species pool and could be found in other habitats
comparisons with other studied coral provinces must take rather than being restricted to the CWC habitat in an obligate
this into consideration (Mastrototaro et al. 2010; Chimienti sense. There are over 1300 known species living on Lophelia
et al., this volume). Similar detailed faunistic studies should pertusa reefs in the NE Atlantic (Roberts et al. 2006), and less
be done in other newly discovered Mediterranean CWC than a half of the species (ca 520 taxa listed in this study) have
habitats that are located in different environmental scenarios been recorded in Mediterranean CWC habitats so far (mostly
(e.g. hydrodynamics, depth, exposure to the Levantine from biodiversity studies of SML) (Bongiorni et al. 2010;
Intermediate Water (LIW)), different seafloor geomorphic Mastrototaro et al. 2010; Vertino et al. 2010; Negri and
features (e.g. submarine canyons, seamounts) and levels of Corselli 2016) (Table 29.1). Consequently, it is reasonable to
disturbance due to anthropogenic activities (e.g. bottom assume that the Mediterranean CWC community is poten-
trawling). Nevertheless, it is clear that Mediterranean CWC tially less rich in species, although additional biodiversity
habitats containing live and dead CWC seem to provide a studies on the benthic and demersal assemblages on different
higher biodiversity of different ecosystemic components CWC sites (e.g. Alborán Sea, Catalan-Provençal-Ligurian
(e.g. meiofauna, macrofauna) than surrounding soft bottoms canyons, SoS) are still needed for detailed and faithful
because these complex habitats act like “oases in the desert” Atlanto-Mediterranean comparisons. In line with this, several
in deep-sea Mediterranean areas (Bongiorni et al. 2010; authors have highlighted that the biodiversity of the deep ben-
Mastrototaro et al. 2010). thic Mediterranean fauna, including that of CWC habitats, is
It has been suggested that Mediterranean CWC habitats lower compared to that of coastal areas where highly diverse
are less diverse than their NE Atlantic counterparts, in benthic communities have been generally reported in threedi-
response to a variety of historical, oceanographic and climatic mensionally complex habitats (Pérès 1985; Boudouresque
factors which conspired in shaping the deep-sea Mediterranean 2004; Emig and Geistdoerfer 2004; Templado 2014).
benthic and demersal fauna (Zibrowius 1980; Fredj and Regarding CWC habitats, the associated communities seem
Laubier 1983; Fredj and Maurin 1987; Bouchet and Taviani to be less biodiverse than those from the Atlantic Ocean.
29.4 A
ssociated Fauna of CWC Habitats to have an important role in the bioerosion of the CWC
in the Mediterranean Sea biocoenosis (Calcinai et al. 2001). The sponge assemblages
and Adjacent Areas of SML display a distinct bathymetric pattern with marked
decrease in species richness with depth (Longo et al. 2005).
29.4.1 Poriferans For instance, S. insignis was preferentially found from 600 to
800 m, while Hamacantha implicans (= H. papillata) from
Sponges are common components of Atlantic and 800 to 1100 m. In the Bari canyon (southwestern Adriatic
Mediterranean CWC habitats, displaying high species rich- Sea), more than 20 sponge species have been found growing
ness and biomass that increase in turn the benthic heteroge- within M. oculata banks (D’Onghia et al. 2015), being the
neity and the number of available microhabitats (Longo massive P. monilifera one of the top-dominant sponges
et al. 2005; Freiwald et al. 2009). Likewise, it cannot be dis- (Freiwald et al. 2009; Bo et al. 2012). Furthermore, D’Onghia
carded that the participation of the sponge fauna in the ben- et al. (2015) also reported S. infestum heavily attacking the
thic-pelagic coupling of local fluxes of dissolved inorganic basal portion of CWC colonies, along with another 11
nutrients (N, Si, C, P) and particulate suspended food species that had never been found before in Mediterranean
(organic Carbon) may significantly contribute to fuel the CWC habitats, namely Prosuberites longispinus, Antho
basal steps of the trophic web in CWC habitats, as it is involvens, Eurypon cinctum, E. topsenti, Biemna partenopea,
known to occur in other marine environments (Maldonado B. tenuisigma, Axinella pumila, Bubaris subtyla, Cerbaris
et al. 2012). curvispiculifer, Hymerhabdia typica and Hexadella pruvoti.
If the functional role of sponges in Mediterranean CWC In CWC habitats of the SoS, Calcinai et al. (2013) listed ten
habitats is far from being fully understood, the knowledge on sponges, mostly encrusting ones and some typical of bathyal
the taxonomic composition of the associated or co-occuring environments (e.g. Janulum spinispiculum, Thrombus
sponge fauna is not much better known for most of the CWC abyssi). Two new records for the Mediterranean Sea such as
provinces in the Mediterranean. One of the earliest studies Characella pachastrelloides and Hamacantha azorica were
specifically on the sponge fauna was addressed by Vacelet also detected in that area.
(1969), who documented the sponge assemblages from Regarding the western Mediterranean, Fabri et al. (2017)
bathyal hard bottoms with CWCs in the Gulf of Lion (NW reported Tretodyctum cf tubulosum, Oopsacas cf minuta,
Mediterranean Sea). Currently, most of the available Hexadella cf crypta and Farrea sp. from the CWC habitat in
information about the sponge fauna of CWC habitats comes the Cassidaigne submarine canyon. In the Sardinian CWC
from SML and Bari canyon CWC provinces. There, sponges province, Taviani et al. (2017) reported a striking paucity of
become the second most abundant component (i.e. number large demosponges which are characteristic and often
of individuals) of the benthic assemblages (Longo et al. dominant components of other Mediterranean CWC banks
2005; Anonymous 2009; Freiwald et al. 2009; Mastrototaro and many slope and seamount hard-bottom habitats (e.g. P.
et al. 2010; Calcinai et al. 2013; Angeletti et al. 2014; compressa, P. monilifera), noticing that most species were
D’Onghia et al. 2015; Taviani et al. 2016), and the encrusting established on dead coral. These authors also documented
desmosponges of the order Poecilosclerida are the most the occurrence of some so far uncommon species such as
common taxonomic group (Longo et al. 2005; Calcinai et al. Clathria anchorata and Acantheurypon pilosella and, all
2013) (Table 29.1). Studies by Longo et al. (2005) and together the Sardinian CWC province is interpreted as a
Mastrototaro et al. (2010) reported the occurrence of 36 putative Mediterranean biodiversity hotspot. The information
species in SML, overgrowing in many cases dead branches relative to the Alborán Sea is limited, based on occasional
of CWC colonies. The assemblage was dominated by small sampling at Chella bank. There, among other species, the
and encrusting sponges including Desmacella inornata and carnivorous sponge Asbestopluma hypogea (= Lycopodina
Sceptrella insignis, and ocassional larger massive species hypogea) has been documented growing on Dendrophyllia
such as Calthropella pathologica, Erylus papulifer as well as cornigera colonies (Aguilar et al. 2011), and the hexactinellids
the flabellates Poecillastra compressa and Pachastrella Asconema setubalense and Sympagella delauzei associated
monilifera. Seven species previously known from other with Lophelia pertusa and M. oculata banks (Pardo et al.
deep-sea habitats, but previously not detected in CWC 2011; de la Torriente et al. 2014) (Fig. 29.2). In the adjacent
habitats, such as E. papulifer, Geodia anceps, Spiroxya GoC, ten large sponges have been listed in CWC habitats of
heteroclita, Antho signata, Crellastrina alecto, Axinella Gazul MV, where Phakellia sp., Haliclona mucosa, A.
cannabina and Hexadella dedritifera, were also described setubalense and Petrosia sp. dominate (Díaz del Rio et al.
for the first time in that CWC province (Longo et al. 2005). 2014; Rueda et al. 2016). A study still in progress on the
Two boring sponges able to excavate the calcareous sponge fauna of MVs in the GoC (Sitjá et al. 2018) has iden-
framework of CWC (Spiroxya levispira and Siphonodictyon tified six additional species growing directly on branches of
infestum) were also found. The latter, occurring exclusively dead coral, namely Desmacella inornata, Poecillastra com-
in Madrepora oculata colonies (Beuck et al. 2010), appears pressa, Anisocrella hymedesmina, Penares euastrum,
Fig. 29.2 Sponges, cnidarians and other invertebrates in cold-water flabellata at a CWC bank of the Gulf of Cadiz (Gazul mud volcano,
coral (CWC) habitats of the Mediterranean Sea and adjacent areas 440 m); (e) The bivalve Acesta excavata together with colonial and
(Gulf of Cadiz): (a) Lollipop-like sponges (Sympagella delauzei) on a solitary scleractinians (mainly M. oculata and Desmophyllum dianthus)
dead coral ground (Cabliers bank, 400 m depth); (b) A small specimen (Dohrn submarine canyon, 420 m); (f) High density of D. dianthus on a
of the sponge Asconema setubalense growing on a coral ground M. oculata framework (Malta trough, 750 m); (g) A colony of
represented by degraded and living Madrepora oculata colonies Leiopathes glaberrima on a dead M. oculata framework with the
(Cabliers bank, 350 m); (c) Dense aggregate of fan-shaped unknown echinoid Cidaris cidaris and lollipop-like sponges (Cabliers bank,
sponges growing on a coral framework of dead and living Lophelia 400 m). (h) Large M. oculata colonies colonised by D. dianthus polyps
pertusa and M. oculata, note the presence of several specimens of and C. cidaris. (Pictures from © Oceana (a–c, g), Oceana©LIFE
undetermined crinoids at the base (Catifas bank, 390 m); (d) Colonies BaĦAR for N2K (f), © Instituto Español de Oceanografía (d), and ©
of L. pertusa and M. oculata together with the hydroid Polyplumaria ISMAR-CNR (e, h))
Characella pachastrelloides and Thrombus abyssi, as well as (Vertino et al. 2010). Within the CWC framework, the
several individuals of L. hypogea growing on boulders solitary polyps of the scleractinian Desmophyllum dianthus
located in the Gazul MV. typically settle on the tissue-barren basal portions of M.
Summarising, ca. 90 sponge species have been detected oculata and L. pertusa playing an important secondary
so far in Mediterranean CWC habitats, but only three species structuring role, especially in some areas (e.g. La Fonera
(D. inornata, Jaspis incrustans and P. compressa) are com- submarine canyons) together with the less abundant
mon to most of these sites (e.g. Catalan-Provençal-Ligurian Stenocyathus vermiformis and Caryophyllia calveri
canyons, SML, SoS, Bari Canyon). Nevertheless, none of (Mastrototaro et al. 2010; Aymà et al., this volume; Lastras
them is specific to CWC, since these species are common in et al., this volume) (Fig. 29.2). Among the most intimate
a large variety of deep-sea habitats. The causes for the poor relationships is that of the actinian Edwardsiella loveni
diversity and low abundance of coral excavating sponges in boring dead branches of L. pertusa (Zibrowius and Taviani
Mediterranean CWC habitats remain elusive. It has been 2005). Black corals (e.g. Leiopathes glaberrima) and
conjectured that it could derive from the difficulty of larvae gorgonians are also common components of these
to reach these calcareous substrates separated by bottoms not biocoenoses and are found both on dead coral ramifications
suitable for skeleton boring fauna (Beaulieu 2001), but it is and among colonies (Tursi et al. 2004; Zibrowius and Taviani
not a strong argument, as calcareous shells are common 2005; Angeletti et al. 2014; Bo and Bavestrello, this volume;
everywhere in deep-sea and they would serve as stepping- see Gori et al., this volume). Noticeably, the calcitic
stones between CWC habitats. Regarding biogeographical Corallium rubrum (precious or red coral), a gorgonian
affinities, most of the sponges found in CWC habitats of the mostly distributed in shallow waters, has been found to occur
Central Mediterranean Sea show an Atlantic-Mediterranean at bathyal depths mixed with CWC in the Strait of Sicily
distribution, with a higher affinity with Boreal fauna, and a from ca 400 down to 1000 m (Freiwald et al. 2009; Costantini
very low percentage of Mediterranean endemic species (13– et al. 2010; Taviani et al. 2010; Knittweis et al. 2016), and in
14%) (Longo et al. 2005; D’Onghia et al. 2015). Moreover, a the Cassidaigne Canyon (Fabri et al. 2017). Three actinians
strong taxonomic differentiation in the composition of the (Amphianthus dohrnii, Sagartia elegans and S. troglodytes)
deep sponge fauna inhabiting soft or hard substrates (e.g. are known to occur as commensal on living portions of M.
coral banks) has been reported, with less than ten species oculata and other anthozoans, similarly to some zoanthids
(e.g. P. compressa, Siphonidium ramosum, Leiodermatium associated with the living coral matrix or with sponges
cf. lynceus, Desmacella annexa, Haliclona flagellifera) (Mastrototaro et al. 2010; Bo et al. 2012).
shared between a CWC habitat off SML and Mediterranean Aside from hydrozoans and anthozoans, the CWC
muddy bathyal bottoms (Pansini and Musso 1991; Longo framework is known to host benthic stages of scyphozoan
et al. 2005). Coronatae medusae (Jarms et al. 2003; Mastrototaro et al.
2010), whereas loose to cemented CWC rubble and other
biogenic hard bottoms generally occurring around CWC
29.4.2 Cnidarians banks host numerous gorgonian species (e.g. Acanthogorgia
hirsuta, Bebryce mollis), scleractinians (D. cornigera) and
Deep-sea anthozoans occurring in Mediterranean CWC hab- antipatharians (Antipathes dichotoma, Parantipathes larix)
itats are mainly represented by structuring scleractinians, (Mastrototaro et al. 2010; Pardo et al. 2011; Angeletti et al.
antipatharians, pennatulaceans and gorgonians (Carpine and 2014; Fabri et al. 2017). Abundant populations of the stolo-
Grasshoff 1975; Zibrowius 1980; Mastrototaro et al. 2013, niferan Scleranthelia rugosa have been reported on giant
2017; Bo et al. 2015; Altuna and Poliseno, this volume; oyster shells (likely Neopycnodonte zibrowii) while the rare
Chimienti et al., this volume) showing no strict endemism actinian Kadophellia bathyalis has been found on dead
and, frequently, with an Atlanto-Mediterranean distribution coral fragments together with the sea anemone Protanthea
(Taviani et al. 2005; Vertino et al. 2014) (Table 29.1). The simplex (Zibrowius and Taviani 2005; Mastrototaro et al.
scleractinians M. oculata and L. pertusa are the main frame- 2010). The adjacent soft bottoms surrounding coral banks
building species of the deep Mediterranean CWC habitats usually host a very peculiar community dominated by pen-
(Fig. 29.2). Nonetheless, approximately 50 anthozoans have natulaceans (such as Kophobelemnon stelliferum and
been recorded so far associated with these bioconstructions Funiculina quadrangularis) and actinians, such as Peachia
(Zibrowius and Taviani 2005; Freiwald et al. 2009; cylindrica (Mastrototaro et al. 2010; Pardo et al. 2011).
Mastrototaro et al. 2010; Pardo et al. 2011; Angeletti et al. Among gorgonians, the only representative in this soft bot-
2014; Bo et al. 2014; Fabri et al. 2014; Lastras et al. 2016; toms habitat is Isidella elongata (Freiwald et al. 2009;
see also Altuna and Poliseno, this volume). Different groups Pardo et al. 2011; Fabri et al. 2014) and some solitary scler-
of anthozoans can be identified based on their role in the actinians can also occur such as Flabellum chunii (Díaz del
benthic community, their degree of intimacy with the Rio et al. 2014) (Fig. 29.3). Sparse rocky hardgrounds
structuring coral framework and their habitat preferences within CWC habitats host numerous anthozoans, including
Fig. 29.3 Common
polychaetes and molluscs of
CWC habitats in the
Mediterrranean Sea and
adjacent areas. (a and d)
Eunice norvegica; (b and c)
Helmutneris flabellicola on
Flabellum chunii; (e and f)
Serpula vermicularis; (g)
Asperarca nodulosa; (h)
Acesta excavata; (i)
Spondylus gussonii; (j)
Delectopecten vitreus; (k)
Epitonium algerianum; (l)
Danilia tinei; (m) Iphitus
tuberatus; (n) Coralliophila
richardi; (o) Coralliophila
squamosa; (p) Babelomurex
sentix. (Pictures from ©
Instituto Español de
Oceanografía (a–g, i, k, l), ©
ISMAR-CNR (h, m–p) and ©
Serge Gofas – Universidad de
Málaga (j))
scleractinians (such as C. calveri, D. cornigera, D. dian- high diverse associated community, including some cnidar-
thus, Thalamophyllia gasti), black corals (L. glaberrima), ians such as D. dianthus, F. quadrangularis and A. dohrnii
alcyonarians (Anthomastus sp.) and those gorgonians that (Maynou and Cartes 2012; Mastrototaro et al. 2017;
also occur on the coral rubble (Álvarez-Pérez et al. 2005; Pierdomenico et al. 2018).
Mastrototaro et al. 2010; Pardo et al. 2011; Lastras et al. Although the hydroid fauna of the Mediterranean Sea is
2016) as well as the bioluminescent and parasitic zoanthid one of the best known in the world (Boero and Bouillon
Isozoanthus primnoidus (Zibrowius and Taviani 2005; Bo 1993; Bouillon et al. 2004), the deep-sea hydroids have
et al. 2014). Black corals and gorgonians are known to form received little attention and the information is mainly
“animal forests” (sensu Rossi et al. 2017) with high-density restricted to the western Mediterranean and adjacent GoC
aggregations along the Mediterranean continental margin (Gili and Ros 1981; Ramil and Vervoort 1992; Moura et al.
usually confining coral banks in the deepest bathyal ranges 2007). The information about CWC associated hydroids is
(Bo et al. 2012, 2015; Bo and Bavestrello, this volume; still very scarce worldwide (Fosså and Mortensen 1998;
Angeletti et al. 2014; Mytilineou et al. 2014; Cau et al. Henry 2001; Buhl-Mortensen and Mortensen 2005; Henry
2015; Deidun et al. 2015; Taviani et al. 2017; Grinyó et al. and Roberts 2007) and the same applies in the Mediterranean
2016; Gori et al., this volume). Other deep-sea gorgonians Sea and adjacent areas, where around 30 species have been
such as I. elongata can form facies with a high density of found so far (Mastrototaro et al. 2010; Lastras et al. 2016)
colonies growing on bathyal muddy environments and a (Table 29.1). This may stem from the fact that most pub-
lished information on Mediterranean CWC habitats derives 29.4.3 Annelids and Phyllogenetically

from ROV observations, that is a useful deep-sea exploration Related Groups
and sampling method but not ideal for characterising an
important part of the associated biodiversity of CWCs, for Few papers are specifically related to polychaetes associated
example the hydroids among other groups of inconspicuous with CWC habitats in the Mediterranean Sea (Sanfilippo
or cryptic organisms. For this reason and/or because of the 2009; Sanfilippo et al. 2013), however substantial informa-
increasing loss of taxonomical expertise, hydroids occurring tion on this group is found in those contributions listing the
in Mediterranean CWC habitats are often reported in a gen- benthic biodiversity of Mediterranean CWC habitats (Tursi
eral way as “hydroids”, without identification at species level et al. 2004; Zibrowius and Taviani 2005; Da Silva 2009;
(Schembri et al. 2007; Bongiorni et al. 2010; Rosso et al. Freiwald et al. 2009; Mastrototaro et al. 2010; Angeletti et al.
2010; Vertino et al. 2010; Angeletti et al. 2014). In addition, 2014; D’Onghia et al. 2015; Taviani et al. 2017; Lastras et al.
most of these and other studies on Mediterranean deep-sea 2016) (Table 29.1). In total, ca. 80 species have been recorded
hydrozoan fauna do not include accurate data about the spe- so far from living CWC grounds but also subfossil ones
cies abundance and their substrate (often also recorded in a (Remia and Taviani 2005; Taviani et al. 2011b), of which
general form such as “corals”). Thus, the real number of Serpulidae accounts for 11 taxa. The occurrence of the poly-
hydroid species known to be associated with Mediterranean chaete species in CWC habitats is very variable, but the euni-
CWC habitats is probably still underestimated (Table 29.1). cid Eunice norvegica is an ubiquitous inhabitant of
The scant available information does not allow to confidently Mediterranean CWC as detected in the Atlantic ones (Tursi
asses whether some hydrozoans are common, rare or specific et al. 2004; Schembri et al. 2007; Da Silva 2009; Sanfilippo
to CWC habitats because further detailed studies are needed. et al. 2013; D’Onghia et al. 2015; Taviani et al. 2017)
In SML, the most common hydroids seem to be Acryptolaria (Fig. 29.3). Other common serpulids in CWC are typical
conferta, Clytia linearis, Halecium labrosum, Hybocodon cf. components of bathyal hard bottoms, including Serpula ver-
prolifer, Laodeicea undulata, Mitrocoma annae, Nemertesia micularis, Filogranula gracilis, Metavermilia multicristata
antennina and N. ramosa (Mastrototaro et al. 2010). In the and Hyalopomatus madreporae (Tursi et al. 2004; Zibrowius
CWC habitats of Gazul MV (GoC), the most common and Taviani 2005; Mastrototaro et al. 2010; Rosso et al.
hydroids are Acryptolaria crassicaulis, A. conferta, Bedotella 2010; Sanfilippo et al. 2013; Angeletti et al. 2014; D’Onghia
armata, Campanularia hincksii, C. gracilis, Streptocaulus et al. 2015; Taviani et al. 2017) (Fig. 29.3). Because of their
cf. pectiniferus, Cladocarpus sinuosus, Cryptolaria pecti- abundance and diversity, serpulids, therefore, play a role as
nata, Diphasia margareta, Lytocarpia myriophyllum, secondary builders in CWC habitats by filling gaps and add-
Modeeria rotunda, Nemertesia falcicula, N. antennina, ing encrusting material with the calcareous tubes they
Polyplumaria flabellata, Zygophylax biarmata and secrete. Nevertheless, the extent of this effect is quite vari-
Zygophylax cf. brownie (Díaz del Rio et al. 2014; Megina able, and it mostly depends on the locality and the species
and Gónzalez-Duarte unpublished results) (Fig. 29.2). Other involved. Thus, serpulid species found in SML are very
studies have indicated the presence of a lower number of abundant, but in turn they are usually small- sized and
species (e.g. Aglaophenia tubulifera, C. pectinata, Halopteris scarcely supply carbonate to the biological framework
catharina, etc.) in coral rubble bottoms and CWC habitats of (Mastrototaro et al. 2010; Rosso et al. 2010). On the other
the Strait of Gibraltar (Ramil and Vervoort 1992) and of La hand, in the CWC communities of the Bari canyon, the dom-
Fonera submarine canyon (Lastras et al. 2016). inant serpulid is the large size S. vermicularis, which is
An important feature of some mentioned hydrozoa is that closely associated with M. oculata (and more subordinately
they are generally non-specific (with a few exceptions) with with L. pertusa and D. cornigera) in building massive and
regard to the substrate selection (Cornelius 1982; Calder very compact aggregates (Sanfilippo et al. 2013).
1991; González-Duarte et al. 2014) and they typically exhibit The interpretation of the errantiate polychaete E. norveg-
a wide bathymetric range, sometimes inhabiting both shallow ica is emblematic because of the difficulty to assess with
and deep-sea habitats (Altuna 2007). Actually, among the 31 confidence the ecological role of deep-sea organisms within
species detected so far in Mediterranean CWC habitats, only CWC habitats. The worm was firstly interpreted as a coral
14 can be considered more common of deep-sea habitats, bioeroder by using its strong jaws to pierce galleries (Glynn
with the family Aglaopheniidae and Lafoeidae showing the 1997), or as kleptoparasite of CWC polyps (Mortensen
highest number of those species (3 and 5, respectively). A 2001). Further studies on NE Atlantic CWC banks unveiled
particular case is Tubiclavoides striatum; a species described a completely different and positive function documenting
in deep-waters of GoC, associated with mud breccia bottoms, that E. norvegica contributes to strengthen the CWC struc-
carbonate chimneys and M. oculata and L. pertusa banks. ture by stimulating the encalcification of their parchment-
Although it was reported as very frequent in this zone, there like tubes into the coral frames (Freiwald et al. 1997; Roberts
are no other records for this species in the world. 2005). Furthermore, E. norvegica enhances coral calcifica-
tion (up to four times in the case of L. pertusa) resulting in (Negri and Corselli 2016), most information on molluscs
branch thickening and anastomosis and facilitating reef associated with CWC habitats is part of more extensive lists
growth and framework strength (Mueller et al. 2013). This on benthic fauna (Tursi et al. 2004; Mastrototaro et al. 2010;
phenomenon is also commonly observed in the Mediterranean Angeletti et al. 2014; Díaz del Rio et al. 2014; Rueda et al.
CWC habitats (Tursi et al. 2004; Mastrototaro et al. 2010). 2016), benthopelagic fauna (D’Onghia et al. 2011) or
The remaining epibionthic polychaetes likely act as opportu- thanatofacies of CWC habitats (Taviani and Colantoni 1979,
nistic commensals or kleptoparasites of CWC (Buhl- 1984; Bonfitto et al. 1994a, b; Remia and Taviani 2005;
Mortensen and Mortensen 2004), although some strict Rosso et al. 2010; Angeletti and Taviani 2011; Taviani et al.
symbionts such as Haplosyllis chamaeleon (mainly with gor- 2011b; Panetta et al. 2013) (Table 29.1). The overall
gonians) or Helmutneris flabellicolla (mainly with Mediterranean deep-sea mollusc fauna is notoriously
Caryophyllia sp. and Flabellum sp.) can be mentioned impoverished with respect to the Atlantic Ocean (Bouchet
(Zibrowius et al. 1975; López et al. 1996) (Fig. 29.3). and Taviani 1992; Sabelli and Taviani 2014), and this
Another striking characteristic of the polychaete assem- obviously extends to the CWC habitats, which are quite
blages inhabiting Mediterranean CWC habitats is the very diverse in the Atlantic (Mortensen and Fosså 2006). At the
few records of Polynoidae, especially when taking into basin scale, the Central Mediterranean is much better known
account that it is the most common family of CWC symbi- than the eastern and western areas (Gofas et al. 2011; Taviani
otic polychaetes worldwide with 12 recorded species (Buhl- et al. 2011a; Angeletti et al. 2014; de la Torriente et al. 2014;
Mortensen and Mortensen 2004). Nevertheless, just two Negri and Corselli 2016). The number of censed species is
Polynoidae species were recorded in Mediterranean CWC higher when based upon extensive bottom sampling (Tursi
habitats, namely Subadyte pellucida and Harmothoe vesicu- et al. 2004; Rosso et al. 2010; Díaz del Rio et al. 2014; Negri
losa (Mastrototaro et al. 2010), and only the latter seems to and Corselli 2016) than that derived of underwater images
be a strict symbiont of cnidarians (Núñez et al. 2015). which fails to spot small-sized and cryptic elements
The polychaete fauna seems to be more diverse in the bio- (D’Onghia et al. 2011; Fabri et al. 2014; Angeletti et al.
genic carbonate rubble around CWC colonies, where ca. 70 2014; Taviani et al. 2017).
species belonging to 32 families have been recorded Over 50 species of molluscs have been reported from
(Mastrototaro et al. 2010), with only 13% of the total inverte- Mediterranean CWC habitats, including coral rubble and
brate species dwelling on living branches. Again, Serpulidae is taphocoenoses (Table 29.1). Nevertheless, most of them are
the most speciose family and is represented by 12 species. The not strictly associated with CWC and some benefit from the
assemblages in the calcareous rubble bottoms are apparently hard substrate and tridimensional complexity provided.
formed of a mixture of species that are also found in the living Some of these species are able to become common and dom-
colonies such as S. vermicularis, Filograna implexa or E. nor- inant in CWC habitats such as the bivalves Bathyarca philip-
vegica and species commonly found in other detritic bathyal piana, Asperarca nodulosa, Delectopecten vitreus, Spondylus
bottoms as well. The number of species recorded from soft gussonii and Heteranomia squamula and the gastropods
bottoms in surrounding areas is comparatively low with 18 Danilia tinei, Putzeysia wiseri and Mitrella pallaryi (Tursi
species belonging to five families (Mastrototaro et al. 2010). et al. 2004; Rosso et al. 2010; Taviani et al. 2011b; Angeletti
Contrary to the CWC colonies, in which a number of species et al. 2014; Díaz del Rio et al. 2014; Negri and Corselli 2016)
were very frequently detected in several localities, no constant (Fig. 29.3). Some common bathyal molluscs inhabiting soft
species can be mentioned for sedimentary environments. bottoms, such as the bivalves Abra longicallus, Karnecampia
Other related taxa are by far less known than Polychaeta in sulcata, Ledella messanensis and Ennucula aegeensis, the
Mediterranean CWC habitats. The presence of Oligochaeta in gastropods Pagodula echinata, or the scaphopod Antalis agi-
these environments is unknown, although this group can be lis could be consistently detected in mobile sediment within
abundant in bathyal soft bottoms in the Mediterranean basin CWC sites (Mastrototaro et al. 2010; Rosso et al. 2010; Díaz
(Baldrighi et al. 2014). Sipunculans were recorded only occa- del Rio et al. 2014; Negri and Corselli 2016). Although not
sionally, always within the sediment surrounding CWC colo- exclusive of such habitats, the epifaunal bivalve D. vitreus
nies (Da Silva 2009; Mastrototaro et al. 2010) but never often occurs at CWC sites (Mastrototaro et al. 2010; Panetta
among the branches, whereas the echiurid Bonellia viridis is et al. 2010; Taviani et al. 2011a; Negri and Corselli 2016).
often seen in muddy coral rubble facies (Hebbeln et al. 2009). Large limid bivalves such as Lima marioni and A. excavata
are ocasionally found associated with CWC habitats (Taviani
and Colantoni 1979; López Correa et al. 2005; Freiwald
29.4.4 Molluscs et al. 2009; Díaz del Rio et al. 2014) (Figs. 29.2 and 29.3).
The giant deep-sea oyster Neopycnodonte zibrowii preferen-
Molluscs represent a diverse component of benthic habitats, tially settles on hard substrates next to CWC banks and
including those conformed by CWC in the Mediterranean sometimes on coral frames themselves (Taviani et al. 2017).
Sea and adjacent areas (e.g. GoC). With few exceptions Although not at all exclusive to CWC habitats, the bivalves
Rocellaria dubia and Coralliophaga lithophagella can be Corselli 2016), but their trophic relationships are presently
found boring or nestling in CWC rubble (Remia and Taviani unknown. Species of fissurellid gastropods of the genus
2005; Díaz del Rio et al. 2014). The Solenogastre Anamenia Emarginula and architectonicids are also recurrent compo-
gorgonophila has been identified from the gorgonacean nents in Atlantic and Mediterranean CWC banks, including
Paramuricea macrospina from the South Malta CWC prov- subfossil occurrences (Remia and Taviani 2005), and possi-
ince (Mifsud et al. 2008), whilst an undetermined nudibranch bly feeding on associated sponges and cnidarians, respec-
has been observed on CWC associated cnidarians in the tively (Gofas et al. 2011). Some small gastropods such as
southeastern Adriatic Sea (Angeletti et al. 2014). Demersal Lissotesta turrita, Anekes sculpturata and Cirsonella romet-
molluscs have been scarcely investigated in Mediterranean tensis are sometimes found in bottoms with CWC and coral
CWC habitats, but the species Onychoteuthis banksi and rubble but their ethology is unknown (Gofas et al. 2011).
Pteroctopus tetracirrhus have been identified around coral
frameworks and hard bottoms at SML (D’Onghia et al.
2011). In general, mollusc assemblages associated with 29.4.5 Crustaceans
CWC host a wider number of species than adjacent bathyal
muddy bottoms. This holds particularly true when coral rub- Crustaceans of Mediterranean CWC habitats have been
ble, soft sediment patches and hard bottoms co-occur addressed in general research on benthic communities (Tursi
(Mastrototaro et al. 2010; Rosso et al. 2010). et al. 2004; Schembri et al. 2007; Mastrotaro et al. 2010;
Only a few molluscs are obligatorially associated with Rosso et al. 2010) or megafauna assemblages (D’Onghia
CWC, and those are all microcarnivores, mostly in the fami- et al. 2010, 2011, 2015; Angeletti et al. 2014; Taviani et al.
lies Epitoniidae, Nystiellidae and Muricidae-Coralliophilinae 2016, 2017; Fabri et al. 2017). A few papers dealt with the
(Oliverio 1989; Taviani et al. 2009). One of the very few spe- suprabenthic and planktonic associated community
cies strictly related to the ‘white corals’ in the Mediterranean (Madurell et al. 2012a) or listed some balanids occurring in
and Atlantic alike is the Coralliophilinae Coralliophila rich- CWC (Relini 1980; Di Geronimo 2010) (Table 29.1). Most
ardi (Fig. 29.3), possibly feeding on both L. pertusa and M. attention has been given to the Central Mediterranean and to
oculata (Taviani and Taviani 1986). As for the nystiellid large crustaceans such as decapods, although some research
Iphitus tuberatus, this amphiatlantic taxon has been docu- included detailed information on small size crustaceans such
mented in the CWC habitats of the Central and western as ostracods and copepods (Rosso et al. 2010; Madurell et al.
Mediterranean and also from submerged Pleistocene CWC 2012a; Sciuto and Rosso 2015). Small size crustaceans seem
taphocoenoses (Taviani and Colantoni 1979; Taviani and to represent an important contribution of the crustacean
Taviani 1986), but not reported thus far from the eastern assemblage, with dominance of copepods (mainly Calanus
basin. The elusive Atlantic nystiellid Iphitus marshalli, helgolandicus and Diaxis pygmaea), euphausiids (mainly
reported from the Alborán Sea (Templado and Villanueva Nyctiphanes couchii), and decapoda larvae (Munida sp.) in
2010; Gofas et al. 2011), is also probably related to deep the planctonic component of CWC habitats (Madurell et al.
scleractinian corals. The gastropods Babelomurex sentix and 2012a). Amphipods (mainly Melphidippella macra and
Coralliophila squamosa (mainly its form ruderatus) have Normanion ruffoi), and mysidacea (Lophogaster typicus)
also been reported from both recent (Oliverio 1989; Taviani also occur but not as dominant components. Only two living
et al. 2009) and subfossil Mediterranean CWC sites (Taviani ostracod species, namely Bairdoppilata conformis and
and Colantoni 1979; Remia and Taviani 2005; Angeletti and Bythocypris obtusata, have been found living in
Taviani 2011), although their cnidarian hosts are still unknown Mediterranean CWC habitats but nearly 30 additional
and possibly exclude white corals sensu stricto (Fig. 29.3). species were found in the associated thanatocoenoses (Sciuto
Iphitus tuberatus is a cnidarian-predatory gastropod relatively and Rosso 2015). Most of these small crustaceans are not
common on living L. pertusa banks in the NE Atlantic and as exclusive of CWC habitats and can be common and dominant
CWC associated Pleistocene fossil in the Mediterranean Sea in different Mediterranean bathyal and pelagic habitats.
(Taviani and Sabelli 1982). Rather interestingly, it has been Decapods are probably one of the best studied crustacean
reported living associated with D. cornigera in the Alborán groups in Mediterranean CWC habitats, with several studies
Sea (Rubio Salazar 1987; Gofas et al. 2011) suggesting a providing faunistic lists and underwater images (Tursi et al.
more generalistic trophic habit encompassing multiple scler- 2004; Schembri et al. 2007; Freiwald et al. 2009; Mastrototaro
actinian corals. With respect to epitoniid gastropods, et al. 2010; D’Onghia et al. 2011; Maynou and Cartes 2012;
Epitonium dendrophylliae has been collected adhering to Angeletti et al. 2014; Taviani et al. 2016, 2017). More than 20
Dendrophyllia spp. (Margelli et al. 1995; Gofas et al. 2011), species have been listed so far, especially for the Central
whose polyps are in all likeness its prey; E. algerianum has Mediterranean CWC habitats (Table 29.1). Nevertheless, in
been reported to occur from CWC habitats of the GoC (Díaz some of these works, some decapods could not be identified at
del Rio et al. 2014; Rueda et al. 2016), and E. celesti also species level, so the decapod diversity is expected to be higher
from the GoC and SML (Díaz del Rio et al. 2014; Negri and (D’Onghia et al. 2011; Fabri et al. 2014). Most of the decapod
species are not linked specifically to CWC, but they benefit Regarding Cirripedia, barnacles benefit from the hard
from the complex and diverse microhabitats provided by cor- substrate provided by CWC and some studies have given
als (Purser et al. 2013a; Maynou and Cartes 2012). The excep- evidence of their occurrence on both CWC colonies
tion is Munidopsis serricornis which is a comensal seemingly (Schembri et al. 2007) and on coral rubble (Di Geronimo
obligate to cnidarians mainly occurring on L. pertusa, but also 2010), whereas others added information on the linkage to
found on Paramuricea or Acanthogorgia in NE Atlantic as some CWC species (Relini 1980; Young 2001). Although
well as in NW Mediterranean (Mortensen 2001; Macpherson some balanids are often attached to CWC, their strict
and Segonzac 2005). The most common species associated association with CWC is still unclear, unlike that of some
with Mediterranean CWC habitats are the pandalids P. martia balanids with shallow water scleractinians (e.g. Adna anglica
and P. heterocarpus, the crab Anamathia rissoana, the anomu- with Astroides calycularis and other species) (Relini 1980).
rans Munida intermedia and M. tenuimana or the xanthiid Some of these balanids are amongst the largest ones occur-
Monadaeus couchii (Fig. 29.4). Other species such as Ebalia ring in the Mediterranean such as Pachylasma giganteum,
nux, Paramola cuvieri and Homola barbata usually occur in documented in the South Malta coral province in the SoS
CWC habitats because of the shelter provided among the coral (Schembri et al. 2007; Angeletti et al. 2011; Deidun et al.
rubble or the presence of sessile species (sponges and cnidar- 2015), or Megabalanus tulipiformis in association with dif-
ians) that are picked up for camouflage. Species of commer- ferent CWC (Relini 1980). Other species that have been pre-
cial interest such as the giant red shrimp Aristaeomorpha viously found are Metaverruca recta on CWC and Scalpellum
foliacea, the blue and red shrimp Aristeus antennatus, the crab scalpellum on antipatharians (Di Geronimo 2010). The bala-
Geryon longipes or the pink spiny lobster Palinurus mauri- nid assemblages inhabiting Atlantic deep-sea corals show a
tanicus also occur, indicating the importance of CWC habitats higher number of species, including the deep species found
for fisheries in adjacent bottoms (Tursi et al. 2004; Mastrototaro in the Mediterranean Sea (Henry and Mc Laughlin 1986;
et al. 2010; D’Onghia et al. 2011; Pardo et al. 2011; Maynou Young 2001; Buhl-Mortensen and Mortensen 2004).
and Cartes 2012) (Fig. 29.4).
Decapod assemblages associated with Mediterranean
CWC habitats seem to be less diverse that in the Atlantic, 29.4.6 Echinoderms
with some associated species occurring in both basins (e.g.
M. tenuimana, Bathynectes maravigna, Polycheles typhlops) Most information available on echinoderms of Mediterranean
and several species only found on Atlantic CWC habitats CWC habitats, including dead subfossil grounds, concerns
(e.g. Chaceon affinis, Eumunida picta, Uroptychus rubrovi- SML, southern Adriatic sites, and the SoS (Tursi et al. 2004;
tattus, Gastroptychus formosus, Pandalus propinquus, Taviani et al. 2005, 2011a; Freiwald et al. 2009; Mifsud et al.
Caridion gordoni, Synalpheus townsendi) (Buhl-Mortensen 2009; Mastrotaro et al. 2010; Vertino et al. 2010; Angeletti
and Mortensen 2004; Cartes et al. 2014). Although the occur- et al. 2014) (Table 29.1). Eight echinoderm species have
rence of CWC is not always linked to a high decapod diver- been detected so far in SML, including the holothuroid
sity (Metaxas and Davis 2005), the number of decapod Parastichopus regalis and the echinoid Cidaris cidaris, the
species is usually higher in CWC habitats than in adjacent latter a common grazer on both live and dead coral branches
soft bottoms (D’Onghia et al. 2010; Maynou and Cartes and generally found between CWC colonies on the smooth
2012; Cartes et al. 2014; Mastrototaro et al. 2017). D’Onghia crusts of the subhorizontal and subvertical substrates as
et al. (2010) showed that most decapods, including some of reported in Atlantic CWC habitats (Stevenson and Rocha
commercial interest (e.g. P. martia, Parapenaeus longiros- 2013) (Figs. 29.2 and 29.4). On adjacent soft bottoms, the
tris), displayed higher densities and biomasses nearby CWC brittle star Amphiura filiformis forms a true facies and the
habitats in SML than further out, because CWC may provide echinoids Brissopsis atlantica mediterranea, Echinus melo
a refuge area for many species often exploited in surround- and Gracilechinus acutus, the asteroid Odontaster mediter-
ing muddy bottoms (Krieger and Wing 2002). Maynou and raneus and the holothuria Mesothuria intestinalis are com-
Cartes (2012) documented 54 species of decapods crusta- mon components in SML. In the Adriatic Sea (Bari submarine
ceans in Isidella elongata facies of the northwestern canyon) C. cidaris seems to be also a common echinoderm
Mediterranean, with higher abundance and biomass of crus- of the CWC habitats, together with E. melo as well as the
taceans than in adjacent areas, and including species of com- widespread A. filiformis in coral rubble bottoms and
mercial interest such as A. antennatus and P. martia. Ophiothrix quinquemaculata generally inhabiting M. ocu-
Similarly, Mastrototaro et al. (2017) reported a higher biodi- lata colonies and other hard substrates (Angeletti et al. 2014;
versity of different taxa, including crustaceans, in I. elongata D’Onghia et al. 2015).
facies located in the Balearic Promontory (western In the SoS, Zibrowius and Taviani (2005) recorded the
Mediterranean) in comparison to similar bathyal muddy bot- sessile suspension feeding holothurian Psolidium complana-
toms lacking I. elongata. tum firmly attached to substrates embedding subfossil skel-
Fig. 29.4 Common decapods and echinoderms of Mediterranean cold- habitat with Lophelia pertusa (Gulf of Cadiz in front of Faro, 495 m);
water coral (CWC) habitats. (a) The decapod Anamathia rissoana on a (f) Dead M. oculata framework with living Desmophyllum dianthus and
Madrepora oculata colony (Nora canyon, 420 m depth); (b) The a high density of unidentified crinoids (Chella bank, 400 m); (g) A large
decapod Munida sp. in CWC rubble colonised by Acanthogorgia L. pertusa colony with the echinoid Cidaris cidaris and the gorgonian
hirsuta (Avempace bank, 370 m); (c) The deep-water lobster Palinurus A. hirsuta (Cabliers bank, 360 m); (h) M. oculata framework with a few
mauritanicus in partially buried CWC remains (Avempace bank, scattered living colonies and high densities of Ophiothrix sp. and
400 m); (d) Scyllarus arctus inhabiting a dead CWC framework with unidentified crinoids (Chella bank, 420 m). (Pictures from © ISMAR-
Acanthogorgia hirsuta and unidentified crinoids (Chella bank, 250 m); CNR (a) and © Oceana (b–h))
(e) High density of the crinoid Leptometra phalangium in a CWC
etal remains of Desmophyllum, Lophelia and Madrepora, irregular echinoids) and grazing (echinoids) echinoderms are
subfossil giant oyster shells and micriticised sponges. Other also common components of the Mediterranean CWC habi-
echinoderms have been reported from the south Malta coral tats. As previously mentioned for the Atlantic CWC habitats
province, i.e., the almost ubiquitous C. cidaris, and the aster- (Mortensen and Fosså 2006), there is no specific echinoderm
oidea Peltaster placenta and Coronaster briareus (Schembri fauna associated with Mediterranean CWC, and most of the
et al. 2007; Mifsud et al. 2009; Deidun et al. 2015; Evans associated species are facultative and common in other deep-
et al. 2016). The crinoid Leptometra phalangium and cidarid sea habitats, with some of them being very widespread spe-
sea urchins were recorded in habitats dominated by the black cies (e.g. A. filiformis) or displaying an aggregation behavior
coral L. glaberrima and coral rubble (mainly of D. cornig- that leads to the formation of dense beds (e.g. Ophiothrix
era) at St. Vito Promontory, offshore the northwestern coast spp.). Most of these echinoderms have an Atlantic-
of Sicily (Bo et al. 2014). Mediterranean distribution or even a cosmopolitan one (e.g.
In the western Mediterranean, similar echinoderms have A. mediterraneus), except O. quinquemaculata (mainly
been detected in CWC habitats of the submarine canyons of Mediterranean) and P. complanatum (Atlantic and previously
the southern margin of Sardinia as well as of those of the unknown in the Mediterranean).
Catalan-Provençal-Ligurian Canyons region, including the
species C. cidaris, E. melo and G. acutus (Fabri et al. 2014,
2017; Taviani et al. 2017; Lastras et al. 2016). In some of 29.4.7 Bryozoans
these canyons (e.g. La Fonera), the ofiuroid Astrospartus
mediterraneus and dense populations of Ophiothrix sp. were Bryozoans from deep waters, including those associated
documented attached to CWC branches (mainly of M. with CWC, have been poorly and occasionally investigated,
oculata) (Lastras et al. 2016). At places, P. placenta was both in the Atlantic Ocean and the Mediterranean Sea. Most
occasionally found within or around CWC banks of these papers usually dealt with taxonomical aspects, and the
areas and the sea cucumber Holothuria forskali was observed biogeographic information is often restricted to the
roaming over or between the CWC (Taviani et al. 2017; geographic locality (often including latitude and longitude)
Lastras et al. 2016). Some ophiuroids and crinoids have also and depth of occurrence (Harmelin and d’Hondt 1982,
been detected in underwater images taken in CWC habitats 1992a, b). Ecological and environmental data including
of southwestern Sardinia, nevertheless these specimens habitat/substratum where colonies lived are usually missing,
could not be identified (Bo et al. 2015). as well as information about other species forming the
In the Alborán Sea CWC habitats of Avempace, Catifas community. Furthermore, only selected CWC areas have
and Cablier banks, C. cidaris and L. phalangium were been investigated in the Mediterranean and mostly in the last
detected in coral rubble bottoms, together with large densities decade. Focusing exclusively on bryozoans occurring in
of Ophiothrix sp. (Pardo et al. 2011; Sánchez-Gallego et al. Mediterranean “white coral” habitats, Rosso and Di Martino
2014) (Fig. 29.4). The CWC associated echinoderms of (2016) listed 61 species (12 cyclostomes, 1 ctenostome and
Chella bank have been studied with more detail, and the 48 cheilostomes) associated with deep water corals, whereas
assemblage includes C. cidaris and Ophiothrix sp. within the Jiménez et al. (2016) reported 36 species on D. ramea
coral banks, as well as C. cidaris, E. melo, G. acutus and H. colonies from deep circalitoral sedimentary bottoms off
forskali in adjacent hard bottoms, while Holothuria tubulosa Cyprus and Menorca Channel. These data show that CWC
and P. regalis are common components of the soft sediments habitats support a lower bryozoan diversity within the
(de la Torriente et al. 2014). Along the Moroccan margin, Mediterranean basin, at present knowledge, in comparison to
CWC habitats of the Melilla Coral Province were studied by shallow-water habitats conformed by cnidarians such as cor-
Hebbeln et al. (2009) but generally most echinoderms (except alligenous bottoms (Table 29.1).
C. cidaris) could not be identified to species level. In the Nevertheless, no assessment hitherto relates to bryozoans
GoC, the echinoderm assemblage occurring in CWC habitats associated with other CWC habitats in the area, although
at Gazul MV was similar as those for the Alborán Sea, but some studies were devoted to bryozoans associated with
also included one of the very few European populations of the Dendrophyllids from the shelf break (Biocoenosis of
amphiatlantic asteroid Hacelia superba (Rueda et al. 2011). Offshore Rocky Bottoms (RL) of Pérès and Picard 1964)
In conclusion, ca. 20 echinoderms have been censed thus and/or mentioned the association of some species with par-
far for Mediterranean CWC habitats, including a high propor- ticular CWC habitats. One of the first studies that included
tion of suspension and filter feeding species (L. phalangium, information on bryozoans associated with Mediterranean
Psolidium complanatum, P. placenta, O. fragilis, O. quin- CWC habitats was published by Gautier (1958), who
quemaculata, A. filiformis and A. mediterraneus) which may recorded 6 species (Scrupocellaria incurvata, Puellina
take advantage from organic matter inputs arriving from the venusta and Herentia hyndmanni, among others) colonising
water column in areas with strong hydrodynamisms where Dendrophylliid coral skeletons from the Gulf of Genoa
CWC generally occur. Sedimentivorous (holothurians and (Fig. 29.5). Gautier (1962) listed a total of 222 species from
Fig. 29.5 Bryozoans
occurring in CWC habitats of
the Mediterranean Sea. (a)
Copidozoum exiguum
(Menorca Channel, 240 m
depth); (b) Scrupocellaria
delilli (Menorca Channel,
190 m); (c) Puellina (G.)
pedunculata (Menorca
Channel, 190 m); (d)
Escharina dutertrei protecta
(Menorca Channel, 190 m);
(e) Tessaradoma boreale
(Sicily Strait, 690 m); (f)
Smittina cervicornis (Bari
Canyon, 306 m); (g)
Escharina vulgaris (Bari
Canyon, 277 m); (h) Herentia
hyndmanni (Santa Maria di
Leuca, 513 m). Scale bars
500 μm (a, c–f, h), 1 mm (g),
1.5 mm (b). (Pictures from ©
Teresa Madurell and © Mikel
Zabala and deposited at
Museu de Ciències Naturals
de Barcelona (a–d) and ©
Antonietta Rosso (University
of Catania) (e–h))
the western Mediterranean but only 16 species (among which Harmelin and d’Hondt (1992c) mentioned species occurring
Escharella ventricosa, Porella minuta and Stephanollona on CWC skeletons, such as Haplopoma sciaphilum and
armata) occurred on coral skeletons. Harmelin (1979) Crepis harmelini on M. oculata and Desmophyllum in the
recorded 19 taxa (13 cheilostomes and 6 cyclostomes, seven SoS and Puellina scripta on M. oculata, L. pertusa and
of which left in open nomenclature but no ctenostomes) col- Caryophyllia cyathus in the Alborán Sea.
onising rock fragments and dead M. oculata colonies in the The first study aimed at identifying and describing bryozo-
SoS (250–750 m depth). Harmelin and d’Hondt (1992a, b) ans associated with CWC was published by Zabala et al.
recorded 152 bryozoans from the Balgim Expedition (1984) (1993) from samples of submarine canyons carving the north-
through the Strait of Gibraltar and nearby areas but, unfortu- ern Catalan margin (180–350 m depth), from where 36 spe-
nately, almost no information on the habitat or substrate was cies (7 cyclostomes and 29 cheilostomes) were reported to
given, except for three cheilostome species that occurred on colonise living and dead Madrepora and Lophelia exposed
CWC skeletons (Lophelia, Desmophyllum). Nevertheless, skeletons. Recently, the discovery of CWC habitats in differ-
ent sectors of Italian waters enhanced the knowledge of their Bryozoans occurring in Mediterranean CWC habitats usu-
associated bryozoans. Surveys in the SML coral province ally grow as small sized encrusters, often developing spot colo-
(Rosso 2003; Taviani et al. 2005; Mastrototaro et al. 2010; nies or small patches (Zabala et al. 1993; Rosso et al. 2010;
Rosso et al. 2010) and along the Bari submarine canyon D’Onghia et al. 2015). Uniserial runners are rare and erect spe-
(Freiwald et al. 2009; Sanfilippo et al. 2013; D’Onghia et al. cies are not common and usually consist of large sized flexible
2015), allowed the record of 33 bryozoans in deep water coral colonies belonging to candiids, whereas erect rigid species are
bioconstructions and neighboring habitats. From these stud- particularly rare. Tessaradoma boreale and Idmidronea species
ies, 19 species (4 cyclostomes, 14 cheilostomes and an are small sized and the only known large colonies belong to
undetermined ctenostome) were reported for SML and the Smittina cervicornis (Fig. 29.5). Most of them have been
same number for the Bari submarine canyon (3 cyclostomes reported as associated with M. oculata and L. pertusa (73 spe-
and 16 cheilostomes), with 5 species shared by these two cies) and only few with D. cornigera (11 species), and occa-
relatively closely spaced localities. Further knowledge on sionally with other corals (one species on Caryophyllia spp.),
bryozoans is sparse in general papers dealing with CWC hab- but none of them seems to be restricted to CWC habitats.
itats (Taviani et al. 2011a, b, 2016, 2017). Indeed, these species have also been reported from a variety of
A total of 74 species (62 cheilostomes and 12 cyclo- habitats (some in the neighborhood of CWC) and substrate
stomes) have been reported so far from CWC habitats in the types (D’Onghia et al. 2015). Most of the CWC associated
Mediterranean Sea and nearby waters subjected to bryozoans have wide bathymetric distributions, being also
Mediterranean influx (GoC) (Table 29.1). Information pri- widespread to mid-outer shelf habitats. Only H. hyndmanni
marily refers to white coral bioconstructions, covering all the and G. pedunculata seem restricted to the very outer shelf and
CWC provinces presently recognised in the Mediterranean the upper slope (Berning et al. 2008; Mastrototaro et al. 2010)
following Taviani et al. (2011a) and also to a few dead coral although extending to some shallow submarine caves (Rosso
bioconstructions, although with some areas investigated in et al. 2013; Sanfilippo et al. 2013) (Fig. 29.5).
more detail than others.
Regardless of the number of collected samples and pub-
lished papers, some areas seem to be species richer than oth- 29.4.8 Brachiopods
ers. The Iberian-Provençal Basin, with a total of 46 species
(Gautier 1958, 1962; Zabala et al. 1993) includes a large part The information on this group is practically limited to some
of the biodiversity of bryozoans associated with CWC habi- punctual records from the Central Mediterranean. In the
tats. A relatively high number of living species (21) has been SML province, Mastrototaro et al. (2010) reported Gryphus
also reported from the southern Adriatic Sea (Freiwald et al. vitreus as a very abundant species on M. oculata and L. per-
2009; Sanfilippo et al. 2013; D’Onghia et al. 2015). In con- tusa coral colonies, and Megerlia truncata on dead
trast, lower species diversity pertain to the northern Ionian Madrepora colonies. Close to SML, Angeletti et al. (2014)
Sea (Rosso 2003; Mastrototaro et al. 2010; Rosso et al. 2010) revealed the existence of cnidarian-rich deep-sea habitats in
and the SoS area (Harmelin 1979), from where 15 and 12 spe- the southern Adriatic Sea (Apulian and Montenegrin mar-
cies have been reported, respectively. Only seven species are gins), with the presence of Novocrania anomala among the
known from the GoC (Harmelin and d’Hondt 1992a, b, c). associated benthic fauna. In the SoS, Zibrowius and Taviani
Finally, occasional records from other areas include two spe- (2005) listed five brachiopod species found on coral ruble
cies from the Alborán Sea (Harmelin and d’Hondt 1992a, b), bottoms of solitary D.dianthus and colonial L. pertusa and
one species from localities in isolated sectors of the Tyhrrenian M. oculata, at times embedded in packstones and frame-
Sea (Taviani et al. 2016) and one species from the Aegean Sea stones. These brachiopods were represented by Megathiris
(Taviani et al. 2011a, b). It is remarkable that the higher val- detruncata, G. vitreus, M. truncata, Novocrania sp. and
ues of biodiversity belong to CWC located within submarine Platidia sp.
canyons, where general environmental conditions presum- Regarding the western Mediterranean, Taviani et al. (2017)
ably favor the settlement and thriving of bryozoans. documented in the Nora canyon (Capo Spartivento canyon
The most recorded species are Herentia hyndmanni, system, Sardinian coral province) a high density of
Scrupocellaria delilii and Glabrilaria pedunculata followed Terebratulina retusa (up to 50 specimens per 0.2 m2) on dead
by Smittina crystallina, Copidozoum exiguum and M. oculata and L. pertusa frameworks and D. dianthus speci-
Stephanotheca arrogata, occurring all throughout the mens, as well as abundant N. anomala and occasional indi-
Mediterranean (Fig. 29.5). Several species, although widely viduals of M. truncata. On the other hand, G. vitreus was
distributed in other habitats of the Mediterranean Sea, have rarely observed, except on soft inter-coral sediment or associ-
been so far recorded in just one CWC province, whereas few ated with dead coral frames. In the Cap de Creus submarine
species have only been found in restricted areas as Hincksina canyon (northwestern Mediterranean Sea), the most common
longispinosa, reported from the Strait of Gibraltar-GoC area brachiopods in CWC communities (dominated by M. ocu-
and Alborán Sea and never recorded eastwards. lata) were also G. vitreus and M. truncata (Madurell et al.
2012b; Domínguez-Carrió et al. 2014). In the Alborán Sea, habitats and seems to be closely associated with the seabed,
M. truncata and T. retusa commonly settle at CWC and hard it is also common in CWC habitats, also in the Atlantic (see
bottoms of the Chella bank, where a total of 6 different spe- for instance Purser et al. 2013b) probably due to trophic rea-
cies co-occur (Llompart 1988; Aguilar et al. 2011; de la sons because zooplankton and small shrimps can be more
Torriente et al. 2014). Most of the reported brachiopod spe- abundant among the colonies (D’Onghia et al. 2012). This
cies are widespread in different circalittoral and bathyal habi-fish is also very common in CWC habitats (dominated by M.
tats so they are not specific of CWC habitats, but it is unknownoculata) at the Nora canyon (Sardinian coral province),
if they may reach higher densities than in hard bottoms at together with Polyprion americanus, large Scorpaena elon-
similar depths. gata specimens, Acantholabrus palloni and Benthocometes
robustus (Taviani et al. 2017), as well as in black coral habi-
tats (dominated by L. glaberrima) at the Malta Escarpment
29.4.9 Fishes (310–315 m) together with Macroramphosus scolopax,
Lepidopus caudatus and P. americanus (Angeletti et al.
As mentioned previously, Mediterranean CWC habitats may 2015) (Fig. 29.6). Close to the Eastern Mediterranean, the
serve as a feeding area, shelter in front of predators and/or information on fish assemblages is limited to the study by
breeding and nursery habitats for fishes, where they generally Mytilineou et al. (2014) who characterised them in CWC
display higher density and diversity values than in adjacent habitats at Kephalonia Island (300–850 m). H. dactylopterus
bottoms (Husebø et al. 2002; Costello et al. 2005; D’Onghia and G. melastomus were the most commonly caught fishes
et al. 2011; Biber et al. 2014). Nevertheless, the functional close to CWC. According to Mytilineou et al. (2014), no
role of the CWC on fish diversity and abundance is still not clear relationship for diet or reproduction was detected
fully understood (Milligan et al. 2016) and data assessing the between H. dactylopterus and CWC and therefore the only
linkage between CWC and fish are still scarce (Purser et al. suggestion, if any, could be related to the shelter provided by
2013b; Biber et al. 2014). Milligan et al. (2016) suggested CWC. Regarding G. melastomus, its preference for CWC
that the importance of Atlantic CWC for fish is species- habitats in relation to hard/mixed bottoms could be due to
specific and depends on the broader spatial context in which feeding, as CWC related bottoms are generally inhabited by
the substratum is found, so this could also apply to the higher amounts of small crustaceans.
Mediterranean CWC communities. In western Mediterranean CWC habitats, information on
Most previous studies on fish communities associated to fishes is also scarce and no detailed studies have been done to
CWCs in the Mediterranean have been done at SML, where date (Reyss 1971; de Lucia et al. 2008; Hebbeln et al. 2009;
Tursi et al. (2004) identified 17 fishes (5 Chondroichthyes Pardo et al. 2011; de la Torriente et al. 2014). At Lacaze-
and 12 Osteichthyes) classified as co-occurrent species Duthiers submarine canyon, the most common fishes in CWC
including the frequent Etmopterux spinax, Galeus melasto- habitats are Scorpaenids (Scorpaena spp.) and Serranids
mus, Benthocometes robustus and Nezumia sclerorhynchus (Polyprion americanus) (Reyss 1971), whereas H. dactylop-
(Table 29.1). In this area, D’Onghia et al. (2010, 2011, 2012) terus, Trisopterus luscus and Trachurus mediterraneus are
found that the most abundant fishes were the teleosts Pagellus the most abundant fishes within an assemblage including 23
bogaraveo, Helicolenus dactylopterus and Conger conger, fish species at Cap de Creus canyon (de Lucia et al. 2008).
as well as the cartilagineous G. melastomus (Fig. 29.6). A Mastrototaro et al. (2017) reported a total of 15 fishes in
remarkable abundance of small sized fishes was detected due aggregations of I. elongata of the Balearic Promontory, docu-
to the recruitment of E. spinax, Merluccius merluccius, menting interesting behaviour patterns for some species
Micromesistius poutassou, Phycis blennoides and H. dacty- including B. robustus, which was observed camouflaging
lopterus. This suggests that SML CWC habitats act as nurs- itself swimming vertically behind the branches of I. elongata.
ery areas, provinding suitable environmental conditions for At Alborán Sea CWC habitats and coral rubble bottoms from
early life stages of those fishes (D’Onghia et al. 2010; Chella, Djibouti and Cabliers banks, the most common spe-
D’Onghia, this volume). Considering the repeated observa- cies are H. dactylopterus, Scorpaena scrofa, M. poutassou,
tions of occurrence in CWC habitats, adult individuals of P. Hoplostethus mediterraneus and P. bogaraveo (Hebbeln et al.
bogaraveo seem to be energetically dependent on the hydro- 2009; Pardo et al. 2011; de la Torriente et al. 2014) (Fig. 29.6).
graphically mediated food production in these habitats In CWC habitats at Gazul MV (GoC), the fish assemblages
(D’Onghia et al. 2012). The significantly high abundance are dominated by similar species than those of the Alborán
recorded for C. conger seems to indicate a preferential distri- Sea (Díaz del Rio et al. 2014).
bution of the species in structurally complex three-dimen- These studies reported, in most cases, fish species that are
sional habitats like those built by CWC (D’Onghia et al. common at similar depths and in different habitat types
2012), as detected for its congener C. oceanicus in western (from soft to hard bottoms), thus the fish fauna occurring in
Atlantic CWC habitats (Ross and Quattrini 2007 in Linley CWC habitats is not exclusive to this habitat type. For
et al. 2015). Although H. dactylopterus uses a wide range of instance, H. dactylopterus is widespread in the whole
Fig. 29.6 Some fishes frequently observed in Mediterranean CWC bank, 250 m); (e) A large specimen of Conger conger close to several
habitats. (a) Macroramphosus scolopax in front of a large colony of the colonies of M. oculata and the large gorgonian Callogorgia verticillata
black coral Leiopathes glaberrima (Chella bank, 360 m depth); (b) (Malta trough, 550 m); (f) Galeus melastomus on a buried dead coral
Pagellus bogaraveo on a Madrepora oculata dominated bank, together framework together with a small Asconema setubalense (Catifas bank,
with several individuals of Hoplostethus mediterraneus (right) and a 400 m); (g) Scorpaena elongata on a M. oculata framework (Cabliers
Cidaris cidaris (center) over a lost fishing longline (Chella bank, bank, 370 m); (h) Phycis blennoides moving on coral rubble bottoms,
320 m); (c) The fish H. mediterraneus close to a large M. oculata with colonies of Lophelia pertusa (front) and Dendrophyllia cornigera
colony, with several C. cidaris in the foreground and background (background) (Chella bank, 430 m). (Pictures from © Oceana (a–d, f–h)
(Chella bank, 340 m); (d) An individual of Aulopus filamentosus lying and from © Oceana©LIFE BaĦAR for N2K (e))
on a dead coral framework with a high density of Ophiothrix sp. (Chella
Mediterranean basin covering a large range of depths ans: Longo et al. 2005; Calcinai et al. 2013; molluscs: López-
(between 40 and 1100 m) and bottom types (Lloris 2015). A Correa et al. 2005; Negri and Corselli 2016; bryozoans:
better understanding of the interactions of CWC with the Zabala et al. 1993; Rosso 2003; fishes: D’Onghia et al. 2012;
associated fish species, biological and ecological processes meiofauna: Bongiorni et al. 2010; Sandulli et al. 2015; deca-
and environmental regulating factors is of crucial importance pods: Capezzuto et al. 2012). Regarding cnidarians, the
as the effects of CWC on fish diversity and/or abundance scarce available information on CWC associated hydroids
varies across CWC habitats (Linley et al. 2015). Nevertheless, hinders our understanding of whether some species are com-
interpreting apparent species-habitat associations must be mon, rare or specific of this habitat within the Mediterranean
done with care taking into account that any assessment of a Sea, and thus accurate data about assemblage composition,
fish species preference will require detailed study on the species abundance and hydroid preferential substrate is
organism over appropriate temporal and spatial scales needed. With respect to deep anthozoans, there are still many
(Milligan et al. 2016). knowledge gaps regarding some taxa, such as stoloniferans,
alcyonarians, corallimorpharians, actinarians, ceriantharians
and zoantharians, due both to sampling constrains because of
29.5 Future Research their small size, fragility or burrowing habits and to
significative taxonomic issues that have led to an
Although many studies on Mediterranean CWC banks have underestimation of their importance in deep-sea communi-
been published in recent years, the information about their ties (see Altuna and Poliseno, this volume). Regarding poly-
associated faunistic communities and the relationships chaetes, future research should include the study of those
between CWC and that fauna is very scarce, especially in the inhabiting live CWC colonies in order to identify potential
western and eastern basins, as well as in the adjacent areas symbiotic relationships (especially Polynoidae), as well as to
influenced by the MOW (e.g. Strait of Gibraltar, GoC) assess the role of Serpulidae species as binders or secondary
(Zibrowius 2003; Tursi et al. 2004; Taviani et al. 2005, 2017; builders in CWC habitats across the Mediterranean basin. To
Freiwald et al. 2009; Mastrototaro et al. 2010; D’Onghia et al. date, neither Platyhelminthes nor Nemerteans have been
2015). Preliminary investigations on biodiversity of CWC recorded from Mediterranean CWC habitats, although fur-
habitats from the Alborán Sea and other Mediterranean areas ther studies devoted to the infauna inhabiting sediments
(e.g. Malta escarpment, off South Creta) as well as from the around these structures might shed some light on the pres-
GoC under the framework of different ongoing projects will ence of both groups. There is also scarce information on the
provide new and needed information on the spatial distribu- relationships of bryozoans and brachiopods with CWC habi-
tion and linkage of associated species across CWC habitats of tats, moreover there are no studies on their preferential sub-
this part of the world (see Knittweiss et al., this volume). strate and microhabitats within the CWC habitat in order to
Future directions should also include the analysis of large determine how strong is their association with CWC species.
scale spatial and temporal patterns as well as the environmen- The functional role of CWC habitats in fish diversity and
tal linkage of the CWC associated fauna, as this type of infor- abundance is still not fully understood and data assessing the
mation is completely absent for the Mediterranean Sea. linkage between CWC and fish species are also needed to
The available faunistic information on the CWC associated detect species-specific patterns (Biber et al. 2014; Milligan
communities is still partial as most of the studies did not com- et al. 2016; D’Onghia, this volume).
bine sampling methods targetting endofauna, epifauna and In general, some groups (peracarid crustaceans, echiu-
demersal fauna in order to obtain a comprehensive and detailed rans, sipunculids, nemerteans, platyhelminths, etc.) have
biological characterisation of each “compartment” of the hardly been considered in previous studies on associated
CWC ecosystem. Nowadays, ROVs are widely used to study CWC biota and the information is nearly absent for the
the characteristics of the CWC habitats. However, although whole Mediterranean CWC habitats. Moreover, there is also
they are very useful and non-invasive deep-sea exploration limited knowledge on prokaryotes that occur in CWC for the
methods, these methods are not ideal for characterising an Mediterranean and no information on protozoans and meio-
important part of the associated biodiversity occurring in these faunal metazoans for mediterranean CWC (for prokaryotes
complex habitats. Hence, to our mind, studies sampling ben- check Weinbauer et al., this volume). Consequently, detailed
thic, planktonic and demersal samples are needed in order to studies on them are still needed. The ethology of CWC
collect the small sized species (mainly for highly biodiverse strictly or preferentially associated taxa (e.g. the gastropods
groups such as molluscs, bryozoans, polychaetes and crusta- Coralliophila richardi and other Coralliophilinae, Iphitus
ceans) and those species that can not be fully identified using tuberatus, and the polychaete Eunice norvegica) should be
external morphological characters (e.g. sponges). explored in-depth to better define their trophic relationships
To date, there are only few studies that focused on specific with the coral host.
species or faunistic groups inhabiting CWC banks in the To complement research efforts addressing these gaps in
Mediterranean Sea (mainly in the central basin) (e.g. porifer- knowledge of CWC associated fauna, priority should also be
given to the investigation of the occurrence and quality of 18, 2006, La Valetta (Malta)-Heraklion (Greece), Supplement to the
Meteor Cruise Report M70/1, Meteor-Berichte, pp 11–5
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various expeditions in the Central Mediterranean of R/V Urania (Cruises Therenia (Bryozoa: Cheilostomata). J Nat Hist 42:1509–1547
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and in the Menorca Channel (INDEMARES) within the LIFE+ ling approach. Deep-Sea Res Part 2 Top Stud Oceanogr 99:134–145
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Cross References Knittweis L, Evans J, Aguilar R, et al (this volume) Recent discoveries
of extensive cold-water coral assemblages in Maltese waters
Lastras G, Sanchez-Vidal A, Canals M (this volume) A cold-water
coral habitat in La Fonera submarine canyon, northwestern
Mediterranean Sea
coral habitat mapping in the Mediterranean: methodologies and
perspectives
Orejas C, Jiménez C, Gori A, et al (this volume) Corals of Aphrodite:
Dendrophyllia ramea populations of Cyprus
Otero M, Marin P (this volume) Conservation of cold-water cor-
als in the Mediterranean: current status and future prospects for
Bo M, Bavestrello G (this volume) Mediterranean black coral communities
improvement
Puig P, Gili JM (this volume) Submarine canyons in the Mediterranean:
a shelter for cold-water corals
D’Onghia G (this volume) Cold-water coral as shelter, feeding and life-
Taviani M, Vertino A, Angeletti L, et al (this volume) Paleoecology of
history critical habitats for fish species: ecological interactions and
Mediterranean cold-water corals
fishing impact
Vertino A, Taviani M, Corselli C (this volume) Spatio-temporal distri-
Fourt M, Goujard A, Chevaldonné P (this volume) Working with visual
bution of Mediterranean cold-water corals
methods, comparison among the French deep-sea canyons
Weinbauer MG, Oregioni D, Großkurth A, et al (this volume) Diversity
Gori A, Grinyó J, Dominguez-Carrió C, et al (this volume) Gorgonian
of bacteria associated with the cold water corals Lophelia pertusa
and black coral assemblages in deep coastal bottoms and continen-
and Madrepora oculata
tal shelves of the Mediterranean Sea
Cold-Water Corals as Shelter, Feeding
and Life-History Critical Habitats 30
for Fish Species: Ecological Interactions
and Fishing Impact
Gianfranco D’Onghia
Abstract in cold-water coral habitats, it should be take into consid-

This chapter is a review of studies that present the role of eration that these habitats are highly impacted in the
cold-water corals as shelter, feeding and life-history criti- Mediterranean and throughout the oceans in general.
cal habitats for fish species in the Mediterranean Sea and Studies on this topic have been reviewed shortly focusing
world oceans. Studies in the Mediterranean have been car- on the Mediterranean Sea where longlining and trawling
ried out both in Madrepora-Lophelia dominated commu- are the main causes of fishing impact.
nities and in coral areas characterised by octocorals and
black corals. Most studies in the northeast Atlantic regard Keywords
Lophelia pertusa reefs, while those in the northwest Cold-water coral · Habitat · Fish · Megafauna · Fishing ·
Atlantic refer to Oculina varicosa, L. pertusa and octo- Impact · Mediterranean
coral species. Octocorals and black corals dominated in
the studies from the northeast Pacific. Most studies show
that the cold-water coral habitats are important for fish
species. In fact, a variety of fish species have been observed 30.1 Introduction
and suggested to benefit from shelter and productive feed-
ing in the complex heterogeneous habitats built by corals. The habitat can be considered as the structural and functional
This is due to the enhanced density of zooplankton as component of the environment that attracts organisms and
potential prey for planktivorous fish and high density of where biological and ecological activities take place
invertebrates between and around corals as food for ben- (Ricklefs 1979; Hayes et al. 1996). The habitat offer to the
thos feeders and scavengers. Moreover, several fish spe- organisms suitable physical and chemical features, food and
cies use cold-water coral habitats as a spawning area and spatial resources, places for courtship, mating and spawning,
nursery. The occurrence of gravid individuals frequently breeding sites and nurseries, places to hide from predators
observed in the coral habitats, as well as the presence of and refuges to escape from adverse environmental condi-
egg masses found deposited on coral stalks and egg cases tions (e.g. Ricklefs 1979 and references therein; Orth et al.
attached to corals or found nested in coral colonies are 1984; Rozas and Odum 1988; Lindberg and Stanton 1989;
clear evidence that several fish species rely on coral habi- Hixon and Beets 1993; Beck 1995; Tupper and Boutilier
tats as a place to spawn and protect offspring. The fish 1995; Langton et al. 1996; Auster et al. 1997; Harvey and
species of families Scyliorhinidae, Sebastidae, Serranidae, Bourget 1997; Lipcius et al. 1998; Sale 2002; Ryer et al.
Berycidae, Zoarcidae, Lotidae, Moridae, Congridae, 2004; Caddy 2007, 2008; Juanes 2007; Wirsing and Ripple
Liparidae seem to be more tightly associated to cold-water 2010; Ryer et al. 2015).
coral habitats. Some fish species of these families obtain Many studies have demonstrated that the structural com-
multiple benefits from their association with cold-water plexity of the marine habitat plays a very important role in
coral habitats, despite being facultative inhabitants. the life history of invertebrate species and fishes, both in
Regarding the occurrence of many commercial fish species shallow (e.g. Orth et al. 1984; Tupper and Boutilier 1997;
Sale 2002; Caddy 2007 and references therein; Juanes 2007
G. D’Onghia (*) and references therein) and deep waters (e.g. Pearcy et al.
Department of Biology, CoNISMa Local Research Unit Bari, 1989; Stein et al. 1992; Caddy 2007 and references therein;
University of Bari Aldo Moro, Bari, Italy Juanes 2007 and references therein; Buhl-Mortensen et al.

https://doi.org/10.1007/978-3-319-91608-8_30
336 G. D’Onghia
2010 and references therein; Miller et al. 2012; Porteiro et al. The first data on fishes associated with CWC in the
2013; Ross et al. 2015). The structural complexity of the Mediterranean Sea were reported in Reyss (1964) for the
marine habitat can be related to the complexity of the geo- Lacaze-Duthiers canyon and Bourcier and Zibrowius (1973)
morphology and substrate: from small-medium scale hetero- for the Cassidaigne canyon. Observations of fish species dis-
geneity due to pits, cobbles, boulders, rocky outcrops, tributed in coral habitats were also reported in Tunesi and
vertical reliefs (Stein et al. 1992; Tupper and Boutilier 1995; Diviacco (1997), Tunesi et al. (2001), Tursi et al. (2004),
Caddy 2007) to large seafloor features, such as seamounts Hebbeln et al. (2009) and Mastrototaro et al. (2010).
and canyons (Porteiro et al. 2013; Fabri et al. 2014; Ross However, the first quantitative data on the effects of CWC
et al. 2015). In addition, habitat complexity can be enhanced habitat on the abundance and size of fishes were provided by
by the architecture of biological structures which range from D’Onghia et al. (2010). Successively, further studies were
natural shell detritus (Caddy 2007), sabellariid worm reefs carried out in the Mediterranean CWC habitats at different
(Gore et al. 1978), amphipod tubes (Auster et al. 1997), pen depths and locations, including canyons, providing new
shells (Kuhlmann 1998), cerianthid anemones (Auster et al. insights into the role of CWC as critical habitats for fish spe-
2003), polychete tubes (Diaz et al. 2003), to seagrass beds cies (e.g. D’Onghia et al. 2011, 2012, 2015a, b, 2016; Bo
(Orth et al. 1984; Stoner and Waite 1990), kelp forests et al. 2011a, 2012, 2015; Fabri et al. 2014; Mytilineou et al.
(Tegner 1993), sponge fields and coral reefs in shallow (Sale 2014; Cau et al. 2017; Mastrototaro et al. 2017).
2002 and references therein) and deep waters (e.g. Freese Irrespective of the mechanistic linkage between CWCs
and Wing 2003; Buhl-Mortensen et al. 2010 and references and associated fish fauna, a review of the studies that show a
therein; Miller et al. 2012). role of CWCs as shelter, feeding and critical life-history hab-
The framework-forming cold-water corals (CWCs) repre- itats for fish species in the Mediterranean Sea and the world’s
sent complex heterogeneous habitats that occur worldwide, oceans is presented here. In addition, information on the fish-
from shallow (from a depth of 40 m in some Norwegian ing impact on these sensitive habitats has also been provided,
fjords) to deep waters, in environments otherwise dominated focusing on the Mediterranean Sea.
by soft sediments (e.g. Reed 2002; Freiwald et al. 2004;
Roberts et al. 2009; Buhl-Mortensen et al. 2010, 2017a). In
the last two decades many studies have investigated the 30.1.1 Structure of This Chapter
megafauna distribution in relation to CWC habitats in north-
east Atlantic (e.g. Fosså et al. 2002; Husebo et al. 2002; This review regards fish species and CWCs, the latter mostly
Costello et al. 2005; Roberts et al. 2005; Söffker et al. 2011; represented by colonial species which live in cold waters,
Purser et al. 2013; Biber et al. 2014; Kutti et al. 2014; have a complex branching morphology and form a habitat on
Milligan 2016; Linley et al. 2017), northwest Atlantic (e.g. the seafloor and hard substrata. A literature search was car-
Reed 2002; Reed et al. 2006; Edinger et al. 2007; Ross and ried out in online libraries, primarily Google Scholar, using a
Quattrini 2007; Sulak et al. 2007; Baker et al. 2012; Quattrini combination of keywords: (1) deep-sea corals, (2) cold-water
et al. 2012), northeast Pacific (e.g. Heifetz 2002; Krieger and corals, (3) fish, (4) megafauna, (5) habitat, (6) nursery, and in
Wing 2002; Stone 2006; Du Preez and Tunnicliffe 2011), addition (7) fishing/fisheries and (8) impact, mostly for the
and in the Mediterranean Sea (e.g. Tursi et al. 2004; D’Onghia Mediterranean Sea. Unpublished papers and those from the
et al. 2010, 2011, 2012, 2016; Bo et al. 2015; Mastrototaro so called “grey literature” have not been included because
et al. 2010, 2017; Chimienti et al., this volume; Rueda et al., these are difficult to obtain and generally not available to
this volume). Although most of the studies have not demon- most readers. Apart from some particular case studies which
strated whether CWCs themselves or only their structural document a clear link between coral presence and fish habi-
complexity are the attracting factors for different life stages tat use, papers regarding canyons and seamounts with the
of the fish fauna (e.g. Auster 2005, 2007; Du Preez and presence of CWCs were also not examined due to the con-
Tunnicliffe 2011; Söffker et al. 2011; Quattrini et al. 2012; founding effect related to these topographic features and
Biber et al. 2014; Kutti et al. 2014; Milligan et al. 2016), sev- CWCs. Relevant studies that detail CWC habitat association
eral investigations have proved a significant role of CWCs as and use by fish species are presented according to the topic
functional habitats for different fish species or a significant of the ecological interaction in two main groups: (1) CWCs
relationship between fish presence and CWC framework as shelter and feeding habitats and (2) CWCs as spawning
(e.g. Koenig et al. 2000; Husebo et al. 2002; Krieger and and nursery habitats. In each of these two groups the results
Wing 2002; Etnoyer and Warrenchuk 2007; Ross and of the different studies have been analysed for the
Quattrini 2007; D’Onghia et al. 2010; Baillon et al. 2012; Mediterranean Sea and for the world’s oceans. The scientific
Henry et al. 2013; Purser et al. 2013; Bo et al. 2015; Cau and common names of the fish species are reported accord-
et al. 2017; Henry and Roberts 2017 and references therein). ing to FishBase (Froese and Pauly 2000).
30 Cold-Water Corals as Shelter, Feeding and Life-History Habitats for Fish Species 337
30.1.2 Terminology densities and smaller sizes. Large specimens of H. dactylop-

terus and P. bogaraveo were exclusively collected in the
The term “shelter” refers to a place within the normal range coral habitat using longline. The blackmouth catshark
of species distribution which allows the protection of indi- (Galeus melastomus) was captured both inside and outside
viduals, irrespective of whether they are juveniles or adults, the CWC area but with large individuals mostly captured in
elsewhere subject to high mortality, mostly due to predation the coral area. Greater abundances in the coral area were also
and/or fishing. obtained for the European hake (Merluccius merluccius), the
The term “feeding habitat” refers to a place within the blue whiting (Micromesistius poutassou), P. blennoides, the
normal range of species distribution which provides food hollowsnout grenadier (Coelorinchus caelorhincus), the
resources to individuals, irrespective of whether they are Mediterranean slimehead (Hoplostethus mediterraneus) and
juveniles or adults. the velvet belly shark (Etmopterus spinax) (D’Onghia et al.
A “life-history critical habitat” can be defined as a part of 2010).
a fish habitat related to breeding, spawning and nursery. This The presence of coral mounds mostly in the north-eastern
does not imply the exclusive or obligate use of the habitat, sector of the SML CWC province seems to influence the
but the absence of this habitat may lead to lower reproduc- large scale distribution of the deep-sea benthopelagic fauna
tion and growth, affecting the renewal of populations. due to higher food availability and a high heterogeneity of
No distinction has been made between “juvenile concen- substrates (D’Onghia et al. 2011). In fact, the greater pres-
tration” and “nursery habitat” or “mature individual concen- ence of corals and sponges in the north-eastern part of the
tration” and “spawning habitat” due to the insufficient data SML coral area might create a refuge for small planktonic
available to make such distinctions possible. and benthic invertebrates, which in turn may be preyed upon
by the mobile fauna observed in the area. Although not quan-
tified, the high concentration of small invertebrates observed
30.2 Ecological Interactions using towed cameras on the north-eastern side of SML, most
Between Fishes and Cold-Water probably represents the attracting factor for the benthope-
Corals in the Mediterranean Sea lagic fauna (D’Onghia et al. 2011). Among fish species,
H. dactylopterus exhibited a clear behavioural pattern of
30.2.1 CWCs as Shelter and Feeding Habitats resting on the seabed in different macrohabitats while
P. bogaraveo seemed to be significantly associated with the
The first clear evidence of the role of CWC habitats as shel- presence of corals (D’Onghia et al. 2011). Further evidence
ter for fish species is reported in Hebbeln et al. (2009). These of a tight relationship between the blackspot seabream and
authors document the presence of the blackbelly rosefish CWC communities is reported in D’Onghia et al. (2012) and
(Helicolenus dactylopterus) seek shelter close and under- Carluccio et al. (2014). In addition, the preferential distribu-
neath the coral frameworks, using a remotely operated vehi- tion of the European conger (Conger conger), the wreckfish
cle (ROV) in an area of the Alborán Sea (western (Polyprion americanus), H. dactylopterus, G. melastomus
Mediterranean), at about 320 m in depth, characterised by and E. spinax in structurally complex habitats like those built
dead coral frameworks with live colonies of Madrepora ocu- by deep-sea corals has been suggested to be related to their
lata and Lophelia pertusa, several Desmophyllum dianthus, feeding habits linked to need for shelter (D’Onghia et al.
abundant Acanthogorgia hirsuta, white gorgonians, black 2012). A close association of C. conger and H. dactylopterus
corals and sponges. Several other fish species, such as the with CWC communities was subsequently observed
lesser spotted dogfish (Scyliorhinus canicula), the greater (Capezzuto et al. 2012; Sion et al. 2012; Maiorano et al.
forkbeard (Phycis blennoides), the boarfish (Capros aper), 2013). The occurrence and behaviour of the sharks, such as
the blackspot seabream (Pagellus bogaraveo) and mac- E. spinax, the gulper (Centrophorus granulosus), the kitefin
rourids, were also observed close to hardgrounds and coral (Dalatias licha) and the bluntnose sixgill (Hexanchus gri-
frameworks with a quite diverse epibenthic organisms seus) in the SML CWC province were also recorded using a
(Hebbeln et al. 2009). benthic lander (Sion et al. 2013).
In the Santa Maria di Leuca (SML) Madrepora-Lophelia The consistent abundance of G. melastomus, C. conger,
CWC province (northern Ionian Sea, central Mediterranean), H. dactylopterus, M. merluccius, P. blennoides and P. bog-
at depths between 300 and 800 m, D’Onghia et al. (2010) araveo was also recorded in five different CWC habitats of
used modified experimental fishing gears and recorded the central Mediterranean, along the continental slope of
greater biomass, densities and sizes inside the coral area than the southern Italy, between the southern Adriatic and
outside, indicating refuge effects. Outside the CWC prov- northern Ionian (D’Onghia et al. 2016). The species
ince, fishing effects were evident due to lower biomass and G. melastomus and H. dactylopterus were the most com-
338 G. D’Onghia
mon fish species caught close to the black coral Leiopathes one of the most commonly associated fish species (Bo et al.
glaberrima and the gorgonian Isidella elongata in the east- 2015; Cau et al. 2017). B. robustus was only observed in
ern Ionian Sea (Mytilineou et al. 2014). Feeding and pro- the close vicinity of large colonies of gorgonians C. verti-
tection relationships with coral habitat have been suggested cillata and antipatharians L. glaberrima and A. dichotoma
for G. melastomus and H. dactylopterus, respectively up to 1 m long in the Bourcart and Cassidaigne canyons
(Mytilineou et al. 2014). H. dactylopterus was also found (Fabri et al. 2014). In particular, three individuals were
together with the longspine snipefish (Macroramphosus observed hiding in C. verticillata fans with their heads
scolopax), silver scabbardfish (Lepidopus caudatus) and pointing downwards (Fabri et al. 2014). Benthocometes
P. americanus in black coral habitats dominated by L. gla- robustus that camouflages itself among the branches of
berrima at the Malta Escarpment (310–315 m) (Angeletti I. elongata swimming vertically was also observed on the
et al. 2015). muddy bottoms between two seamounts east of Ibiza
Linley et al. (2017), using baited cameras on autono- (Balearic Sea) (Mastrototaro et al. 2017). According to
mous benthic landers on coral mounds and off the mounds these authors I. elongata forests also act as trophic areas
in the immediate surrounding area in the SML CWC prov- where many species, such as G. melastomus, E. spinax,
ince, revealed fish abundance higher within the coral sta- M. merluccius, M. poutassou, P. blennoides, H. dactylop-
tions but no significant difference in fish diversity between terus, H. mediterraneus and the four-spot megrim
coral and non coral areas. However, C. conger was observed (Lepidorhombus boscii), find preys swimming among the
with much higher density within the coral areas. Faster colonies or climbing on them. Contrary to these observa-
arrival and higher peak numbers also indicate a greater tions, Cartes et al. (2013) pointed out a rather low capacity
abundance of H. dactylopterus in the coral habitat than in of I. elongata facies in forming habitat for megafauna on
the reference area. Although P. bogaraveo was often muddy bottoms of the Mediterranean slope.
observed in both coral and non coral habitat, its abundance
estimation could be largely biased due to the fast swim-
ming of the different individuals. 30.2.2 CWC as Spawning and Nursery Habitats
In the south Tyrrhenian Sea, in a rocky area character-
ised by the presence of the black coral Antipathes dichot- Fish species observed using the coral habitat for reproduc-
oma, at depths between 90 and 132 m, the labrid Lappanella tion have been recorded in the Mediterranean Sea. Hebbeln
fasciata was observed hidden between the coral ramifica- et al. (2009) observed egg capsules of Scyliorhinus (most
tions (Bo et al. 2011a). In the same geographic area, in a probably S. canicula) on colonies of L. glaberrima at 647 m
coral garden made up of arborescent colonies of gorgonians and 452 m on El Idrissi Bank (Alborán Sea).
(Callogorgia verticillata, Paramuricea clavata, D’Onghia et al. (2010) collected gravid and near-gravid
Paramuricea macrospina, Bebryce mollis, Villogorgia individuals of H. dactylopterus in the SML CWC province,
bebrycoides, Corallium rubrum, and Leptogorgia sarmen- suggesting the presence of a spawning area. The shark E.
tosa) and antipatharians (A. dichotoma, Antipathella sub- spinax was almost exclusively caught inside the coral area
pinnata and Parantipathes larix), between 70 and 130 m with a noteworthy number of small individuals. The remark-
depth, in the Gulf of St. Eufemia, the occurrence of L. fas- able abundance of juveniles both in E. spinax and the teleost
ciata, John dory (Zeus faber), M. scolopax, red bandfish fish M. merluccius, M. poutassou, P. blennoides and H. dac-
(Cepola macrophthalma), H. dactylopterus, forkbeard tylopterus would suggest that the SML CWC province acts
(Phycis phycis) and the shark nursehound (Scyliorhinus as a nursery area for these deep-water species which find
stellaris) was recorded (Bo et al. 2012). suitable environmental conditions and refuge from fishing in
A school of C. aper (erroneously reported as M. scolopax) their early life stages (D’Onghia et al. 2010). The presence of
was observed among the coral colonies of P. larix, between maturing and mature individuals, both females and males, as
100 and 200 m, on rocky outcrops located southeast of the well as post-reproductive individuals of G. melastomus,
Island of Montecristo (Tuscan Archipelago, Tyrrhenian Sea) C. conger, H. dactylopterus, M. merluccius, P. blennoides,
(Bo et al. 2014b). P. bogaraveo, although with different percentages, in five
Various fish species were observed hiding among the CWC sites along the continental slope between the southern
black coral L. glaberrima on a rocky bank with presence of Adriatic and northern Ionian, indicates that these sites act as
other coral species (C. verticillata, B. mollis, A. hirsuta, P. spawning areas, representing a potential “renewal network”
larix and A. dichotoma), at depths between 186 and 210 m, for the fish populations (D’Onghia et al. 2016).
off the south-western coasts of Sardinia (western On a rocky bank dominated by the antipatharian
Mediterranean): S. canicula, the swallowtail seaperch L. glaberrima, off the south-western coasts of Sardinia
(Anthias anthias), M. scolopax, Z. faber, L. fasciata, (western Mediterranean), at depths between 186 and 210 m,
Trachurus sp., and Benthocometes robustus, the latter being eight specimens of the shark S. canicula were observed
moving on the muddy bottom near the rocky elevations and apparently degraded and old capsules), provide support that
within the coral branches (Bo et al. 2015). A total of 743 the coral forest from SW Sardinia can serve as nursery
egg cases of this shark were observed, at different stages of grounds for S. canicula as it has been repeatedly used by
maturation, on the colonies with some corals lacking eggs. this shark (Cau et al. 2017).
In particular, among 244 colonies of L. glaberrima exam- Egg capsules of Scyliorhinus sp. (erroneously reported as
ined, 148 (61%) hosted egg cases (five capsules per colony, G. melastomus) have been recorded anchored to the branches
on average), and one, 2 m tall, hosting 44 capsules of S. of the bamboo coral I. elongata in the Balearic Sea
canicula and one egg case of skate (Bo et al. 2015; Cau (Mastrototaro et al. 2017). Images of fish species and eco-
et al. 2017). The presence of egg capsules at different stages logical interactions in Mediterranean CWC habitats are
of development (i.e from capsules hosting embryos to reported in the Fig. 30.1.
Fig. 30.1 Fish species and

ecological interactions in the
Mediterranean CWC habitats:
(a) Helicolenus dactylopterus
in coral framework habitats
close to Madrepora oculata
colonies; (b) Some specimens
of Hoplostethus
mediterraneus in coral rubble;
(c) Pagellus bogaraveo in the
SML CWC Madrepora-
Lophelia province; (d) P.
bogaraveo near to hardground
with M. oculata colonies; (e)
Concer conger in the SML
CWC Madrepora-Lophelia
province; (f) C. conger in
Madrepora-Lophelia habitat
off Tricase (central
Mediterranean); (g) Polyprion
americanus in the SML CWC
Madrepora-Lophelia
province; (h) Merluccius
merluccius in Isidella
elongata habitat; (i) an egg
capsule of Scyliorhinus sp.
and Anamathia rissoana on I.
elongata; (j) Benthocometes
robustus among the branches
of I. elongata. (a, d) Photo
copyright and courtesy by ©
OCEANA ©LIFE BaĦAR for
N2K; (b) From C. Orejas ©
MEDWAVES/ATLAS project;
(c, e–g) Photo © by
Department of Biology,
University of Bari (CoNISMa
ULR); (h–j) Photo copyright
and courtesy by © OCEANA
340 G. D’Onghia
30.3 E
cological Interactions Between Fish whereas S. viviparus and B. brosme were observed both in
and CWCs in the Oceans coral and reference habitat. This latter was the most numer-
ous species attending the bait with much higher density
30.3.1 CWCs as Shelter and Feeding Habitats within the coral areas.
In relation to the abundant presence of benthic inverte-
30.3.1.1 Northeast Atlantic brates (mostly Munida spp.) and plankton, several authors
Data on the presence of the fauna associated with CWC hab- suggested that the reefs act as sites of increased food avail-
itats dates back to studies carried out in the first half of the ability, providing fishes with refuge from predators and habi-
twentieth century as reported in Jensen and Frederiksen tat from which to ambush prey (Mortensen et al. 1995;
(1992). In particular, these authors collected a small speci- Husebo et al. 2002; Jonsson et al. 2004; Costello et al. 2005;
men (80 mm) of the Norway redfish Sebastes viviparus Kutti et al. 2014). The benthic fish species, such as tusk,
trapped in a coral block recovered from Lophelia pertusa preyed predominantly on epibenthic decapods, such as
reefs on the Faroe shelf. Off Norway, Mortensen et al. (1995) Munida spp. and Lithodes maja (Husebo et al. 2002; Kutti
identified five fish species from Lophelia reefs: the saithe et al. 2014), while redfish are known to be planktotrophic
Pollachius virens (mostly observed feeding), the tusk Brosme predators and the bioherms may enhance the amount of zoo-
brosme, S. viviparus and the golden redfish Sebastes marinus plankton available to these fishes (Mortensen et al. 1995;
as the most common fish in the living Lophelia zone, and the Buhl-Mortensen et al. 2017a).
Atlantic cod Gadus morhua. Sebastes spp., ling (Molva In Lophelia coral reefs explored from the Faroe-Shetland
molva) and tusk were mostly captured on the Lophelia reefs Channel to Porcupine Seabight, Sebastes sp. and M. molva,
compared to non-reef areas (Furevik et al. 1999 in Fosså followed by B. brosme, dominated the fish fauna at Hurtside
et al. 2002; Husebo et al. 2002). The presence of tusk and wreck (Costello et al. 2005). Brosme brosme was also
Atlantic wolffish (Anarhichas lupus) among the dead coral observed at Hatton Bank, where it solely occurred in the
framework was also recorded at the Sula Reef Complex coral framework habitats resulting in a highly significant
(Norwegian Shelf) (Freiwald et al. 2002). G. morhua and relationship (Biber et al. 2014). The presence of the North
vahl’s eelpout (Lycodes vahli) were preferentially associated Atlantic codling (Lepidion eques), hiding beneath colonies
to Lophelia reef in the Kosterfjord (between Norwegian and of L. pertusa, M. oculata, and Antipatharia, was recorded
Swedish waters) (Jonsson et al. 2004). Costello et al. (2005), using an ROV in the deep-water coral province of Porcupine
using video systems, identified S. viviparus (hovering, hid- Bank, on the Irish continental margin (Wheeler et al. 2005a).
ing, resting on the seabed, feeding) as the most abundant fish The fish L. eques, H. dactylopterus, C. monstrosa and
on top of the reef at Sula Ridge and P. virens (actively swim- G. melastomus, were observed in different types of macro-
ming, feeding) as the dominant fish at the Tautra Reef; G. habitat, including coral rubble, coral framework and rock
morhua as the dominant species at Säcken Reef (Kosterfjord), macrohabitats on Hatton Bank (Roberts et al. 2008).
over the transitional and coral debris areas; the poor cod Lepidion eques was also the most common species recorded
Trisopterus minutus (hiding), B. brosme (resting on the sea- using an ROV on Twin Mounds and Giant Mounds, which
bed, feeding) and A. lupus (resting on the seabed) were most are situated 9 km apart on Porcupine Bank (Söffker et al.
frequently recorded in association with the coral reef habitat 2011). It always occurred a few cm above bottom and was
(Costello et al. 2005). Redfish (Sebastes sp.) sheltering near significantly more active on the reefs than on sedimentary
sponges was also observed using a benthic photo-lander at habitats. In this study area, two fish species were particularly
the Sula Ridge reef complex (Roberts et al. 2005). Using associated with coral habitats: Guttigadus latifrons and the
longline in the Træna Deep marine protected area and adja- false boarfish Neocyttus helgae. The former was mainly
cent areas of the Norwegian continental shelf, Kutti et al. found amongst dense living coral thickets and was not
(2014) found higher abundances of B. brosme, Galeus melas- observed in non coral habitats, the latter was found predomi-
tomus and Chimaera monstrosa in coral habitats than in non nantly on structural habitats provided by dead corals (Söffker
coral ones, most probably due to shelter and feeding reasons. et al. 2011). Lepidion eques showed a significantly higher
Subsequently, Kutti et al. (2015), using a towed video system abundance at coral framework patches in Belgica Mound
in the same study areas, observed S. viviparus and B. brosme Province where individuals were observed hiding under-
associated with the CWC and sponge habitats at all the spa- neath the coral framework but also frequently occurred in
tial scales examined. However, none of the species examined non coral areas, where they were particularly associated with
were confined to a single habitat. Linley et al. (2017), using boulders (Biber et al. 2014). The species feeds mainly on
baited cameras on autonomous benthic landers on coral crustaceans and polychaetes, which might explain its fre-
mounds and off the mounds in the immediate surrounding quent occurrence near CWC reefs as these supports a higher
area, detected fish abundance higher within CWC areas than macrofaunal biomass than surrounding soft sediments (Biber
in surrounding areas. P. virens was unique to the coral area, et al. 2014). Helicolenus dactylopterus was also commonly
observed at Rockall Bank sitting relatively motionless on top Galway Mound (Belgica Mound Province) where L. eques
of corals. The association of this fish with coral framework was by far the most common fish, followed by P. blennoides
was explained by the fact that it is considered a protection (Lavaleye et al. 2017).
seeker (Biber et al. 2014). Video surveys carried out from the Azores to the Canary
Using bottom trawl, the capture of the birdbeak dogfish Islands revealed the circalittoral Lappanella fasciata and the
Deania calcea, G. melastomus, C. monstrosa and the upper bathyal Benthocometes robustus closely associated to
angler Lophius piscatorious from areas characterised by biogenic habitats made up of CWC (e.g. Antipathella spp.,
the presence of L. pertusa, M. oculata and other CWC on Acanthogorgia armata, Callogorgia verticillata,
Hatton Bank was also reported by Durán-Muñoz et al. Dendrophyllia alternata, Leiopathes spp.) and large hydro-
(2009). Along the rugged bottom of the rocky outcrop, zoans (Gomes-Pereira et al. 2017). Individuals of these two
high catches per unit effort of the adult fraction of vulner- fish species were shown swimming inside or close to CWC,
able deep-water sharks and Lotidae fish were obtained moving in and out of corals three-dimensional structures, as
using longline in coral areas (Durán-Muñoz et al. 2011). well as maintaining position in relation to the corals or
On the Mingulay Reef Complex, a seascape of Lophelia hydroids. The swimming position indicates behavioral adap-
reefs off western Scotland, the mean abundance of G. tations to coral-cryptic behavior, suggesting that CWCs and
melastomus was significantly higher in trawl sets located large hydrozoans provide shelter from predators, current
nearer a coral reef than those located further away, sug- avoidance and preys for both fish species (Gomes-Pereira
gesting that this shark is locally enhanced near coral habi- et al. 2017).
tats (Henry et al. 2013). Scyliorhinus canicula was also
observed resting among Lophelia colonies on the Mingulay 30.3.1.2 Northwest Atlantic
Reef Complex (Henry et al. 2013). In this geographic region, off the south-eastern United States,
Video footage on demersal fish and substratum types was two types of deep-water coral reefs are formed by the scler-
taken from Logachev Mounds, Rockall Bank and Hebrides actinian corals Oculina varicosa, on the shelf, and L. per-
Terrace Seamount (Milligan et al. 2016). Significant differ- tusa, on the slope (Reed et al. 2005). Schools of thousands of
ences in community composition between all regions, within small individuals of the red barbier (Baldwinella vivanus)
each region at scales of 20–3500 m, and between CWC and were observed to swim among the branches of O. varicosa
non CWC substrata were detected. Sebastes sp. (mainly S. corals for shelter and/or for feeding on the invertebrates liv-
viviparus) was closely associated with CWC reef substrata at ing within (Reed 2002). Oculina reefs were observed as
Rockall Bank. N. helgae was significantly more likely to feeding grounds for gag (Mycteroperca microlepis), scamp
occur in coral areas at the Hebrides Terrace Seamount. The (Mycteroperca phenax), snowy grouper (Hyporthodus nivea-
species L. eques, C. caelorhincus and H. dactylopterus tus) and other fish including black seabass (Centropristis
occurred on coral reefs and transitional substrata and their striata), red grouper (Epinephelus morio), speckled hind
relative abundances were significantly affected by depth. (Epinephelus drummondhayi), warsaw grouper (Hyporthodus
The results of this study suggest that the importance of nigritus), Atlantic goliath grouper (Epinephelus itajara),
CWCs to fish is species-specific and is related to the broader longfin yellowtail (Seriola rivoliana), greater amberjack
spatial context in which this type of substratum is present (Seriola dumerili), red porgy (Pagrus pagrus), Northern red
(Milligan et al. 2016). snapper (Lutjanus campechanus), grey snapper (L. griseus),
From in situ observations using baited cameras, fish spe- little tunny (Euthynnus alletteratus), ocean sunfish (Mola
cies diversity was higher within the coral habitats than in mola), giant manta (Manta birostris), tiger shark (Galeocerdo
reference habitats of the Belgica Mound Province and the cuvieri) and scalloped hammerhead (Sphyrna lewini) (Reed
Bay of Biscay (Linley et al. 2017). The majority of sightings 2002). The most common larger grouper observed in 2003
in the former region were of five dominant species that were were E. morio and M. phenax, although a few individuals of
present in both habitat types: the bluntnose sixgill shark H. niveatus and M. microlepis were also present (Reed et al.
Hexanchus griseus, Synaphobranchus kaupii, L. eques, the 2005). A large male of M. phenax was photographed on O.
common mora Mora moro and Phycis blennoides. varicosa bioherm at 80 m (Reed and Ross 2005). The ROV
Deployments in the latter region were dominated by the surveys on fish assemblages and benthic habitat inside and
same actinopyterygian species as the former: S. kaupii, L. outside the Oculina Habitat Area of Particular Concern
eques, M. moro and P. blennoides. The authors report that (OHAPC) off eastern Florida revealed grouper densities
while CWC reefs have a positive effect on fish diversity and/ (mainly Mycteroperca spp., Epinephelus spp., Serranus
or abundance, this effect varies across Europe’s reefs mainly spp.) significantly higher on the most structurally complex
as a consequence of the different time of year, depth and habitats (live O. varicosa, standing dead O. varicosa and
topography. Temporal variations in the abundance of several rock outcrops) compared to the less complex ones (pavement
species were also observed in the CWC community on and rubble) (Harter et al. 2009).
342 G. D’Onghia
In the regions of Lophelia reef habitats off the south- deep reefs of the south-eastern U.S., the new species of myx-
eastern United States (Blake Plateau, the Straits of Florida inid fish Eptatretus lopheliae was videotaped and caught in
and eastern Gulf of Mexico), surveyed using submersibles close association with Lophelia reef habitat (Fernholm and
and ROV, the most abundant fish species were H. dactylop- Quattrini 2008). Successively, Ross and Quattrini (2009)
terus and the morid cod (Laemonema melanurum), followed surveyed fishes in nine deep reef study areas along the south-
by the alfonsino (Beryx decadactylus), the western roughy eastern U.S. slope. Fish assemblages at the North Carolina
(Hoplostethus occidentalis), the American conger (Conger sites were different from the sites to the south and there was
oceanicus) and the wreckfish (Polyprion americanus) (Reed a large amount of variability in species abundance and distri-
and Ross 2005; Reed et al. 2006). H. dactylopterus and L. bution patterns among the different sites. Laemonema bar-
melanurum were also found to be common in sinkhole and batulum, L. melanurum and H. dactylopterus were abundant
bioherms on the southern edge of the Pourtalès Terrace and consistently observed during the majority of North
(south Florida), even though these sites are mainly character- Carolina dives. C. oceanicus and B. decadactylus were also
ised by stylasterid corals, octocorals, sponges, ascidians and abundant indicator species. Other species that contributed to
lack the scleractinian corals L. pertusa and M. oculata (Reed fish assemblage differences included H. occidentalis, D.
et al. 2005). Schools of ~ 50–100 P. americanus, were rugosa and Idiastion kyphos and the chain catshark
observed on several submersible dives in May 2004 and Scyliorhinus retifer. In the Cape Fear area, N. sclerorhynchus
again at the same site in April 2005 (Reed et al. 2006). and P. americanus were abundant, contributing to the dis-
Wenner and Barans (2001) (in Reed et al. 2006) noted that similarities between this site and others. Ross and Quattrini
wreckfish individuals were frequently seen on these reefs. (2009) suggested that fish community structures were asso-
Specimens of anglerfish Chaunax stigmaeus, Lophiodes ciated with the size, profile and complexity of the deep reefs.
beroe, Lophiodes monodi, and a single specimen of Sladenia Among the fish species examined by Quattrini et al. (2012),
shaefersi sitting on beds of dead coral L. pertusa rubble were B. decadactylus and C. oceanicus were most frequently
observed in dives performed by submersible in the same geo- observed near the top of the coral mound in the presence of
graphic area (Caruso et al. 2007). high vertical profile, live coral coverage and topographic
The demersal fish fauna from hard substrate and Lophelia complexity, most probably in relation to their enhanced feed-
coral biotope in the northern Gulf of Mexico (Vioska Knoll) ing and refuge opportunities. L. melanurum was often
was investigated by submersible (Sulak et al. 2007). Large observed in moderate profile habitats and not often in live
mobile schooling fishes dominated at 325 m in depth (the coral habitats. Transient species, such as H. dactylopterus
barrelfish Hyperoglyphe perciformis, the Darwin’s slime- and L. barbatulum were most observed on the mound slope
head Gephyroberyx darwini and H. niveatus) together with and base with moderate complexity. P. americanus and N.
sit-and-wait ambush mesocarnivores H. dactylopterus and sclerorhynchus exhibited the least affinities for a particular
the ambush predator C. oceanicus. On the 500 depth horizon type of habitat. Quattrini et al. (2012) concluded that certain
C. oceanicus, Laemonema goodebeanorum, H. dactylop- reef-associated species seem to be habitat specialists whereas
terus, H. occidentalis, the Atlantic thornyhead Trachyscorpia others are habitat generalists.
cristulata, the thorny tinsel fish Grammicolepis brachiuscu- Northward, the deep-water gorgonian corals Primnoa
lus were most frequently observed. G. brachiusculus, a mor- resedaeformis and Paragorgia arborea in the north-east
phologically very specialised epifaunal picker, appears to be Channel (Nova Scotia, Canada) were considered as preferred
highly associated with Lophelia reefs. habitats of redfish (Sebastes spp.) providing shelter against
Ross and Quattrini (2007) used a submersible to describe strong near-bottom currents and predators (Mortensen et al.
the degree of habitat specificity of the fishes in prime 2005).
Lophelia reef habitat, transition reef and off reef in eight
areas on the south-eastern United States. They found distinct 30.3.1.3 Central Eastern Atlantic
fish assemblages in prime reef and transition reef habitats In this geographic region, during the ROV video surveys car-
compared to off-reef habitats, suggesting that deep reefs host ried out on coral mounds, along the Angola margin (West
unique fish communities. The prime reef fish assemblage Africa), high abundance of Zoarcidae fish was observed in
was characterised by L. melanurum, the rough tip grenadier the living and dead Lophelia coral framework (Le Guilloux
Nezumia sclerorhynchus, B. decadactylus and H. dactylop- et al. 2009). Their absence in the surrounding sediments and
terus. Some species, such as the swallowtail bass Anthias observed hiding behaviour indicated potential habitat selec-
woodsi, B. decadactylus, C. oceanicus and the cutthroat eel tivity. Other species associated with corals were Chaunax
Dysommina rugosa, showed specificity to reef habitats. In sp., Lophius sp., H. dactylopterus and G. darwini (Le
addition, they found three new fish species (McCosker and Guilloux et al. 2009).
Ross 2007; Fernholm and Quattrini 2008; Nielsen et al. Among the six fish species observed in the Lophelia reef
2009). Among the characteristic fishes associated with the on the Ghanaian shelf (Gulf of Guinea), the most common
were H. dactylopterus, the western softhead grenadier near several sea whips in the Gulf of Alaska (Krieger 1993).
Malacocephalus occidentalis and the blackfin sorcerer Hundreds of rockfish individuals, mainly Pacific ocean
Nettastoma melanorum. These fish were often found hiding perch, were observed inhabiting a “forest’” of attached sea
among blocks of dead coral (Buhl-Mortensen et al. 2017b). whips, Halipteris willemoesi, during night deployments of
Images of fish species and ecological interactions in Atlantic the ROV in Pribilof Canyon (Bering Sea) (Brodeur 2001).
CWC habitats are reported in the Fig. 30.2. During the day, individuals of S. alutus were seen above the
“forest”, where they were apparently feeding on dense
30.3.1.4 Northeast Pacific swarms of euphausiids, indicating that these fish utilise food
In a photograph taken by a submersible, an aggregation of resources in the canyon during the day and are associated
adult Pacific ocean perch (Sebastes alutus) was observed with the sea whip habitat at night during periods of inactivity.
Fig. 30.2 Fish species and

ecological interactions in
Atlantic CWC habitats: (a)
Redfish (Sebastes marinus) in
the L. pertusa reef; (b, c)
Sebastes spp. in Lophelia reef
and sponge ground; (d)
Gadus morhua in Lophelia
reef; (e) Brosme brosme in
Lophelia reef; (f) Brosme
brosme feeding on a smaller
fish caught on the reef
(probably a Lepidion sp.); (g)
Helicolenus and Eumunida
picta in Lophelia habitat; (h)
Phycis blennoides in Lophelia
habitat; (i) Galeus
melastomus and Mora moro
close to CWC habitat; (j)
Hexanchus griseus in
Lophelia habitat. (a) Photo ©
Marine Research Institute of
Iceland, courtesy of Stefán
Áki Ragnarsson and Steinunn
Hilma Ólafsdóttir (from
CoralFISH Gallery); (b–e)
Photo © Institute of Marine
Research (Norway), courtesy
of Jan Helge Fosså and Tina
Kutty; (f) Photo © National
University of Ireland
(Galway), courtesy of
Anthony Grehan (from
CoralFISH Gallery); (g)
Photo © and courtesy of the
U.S. Geological Survey; (h, j)
Photo © and courtesy of
OceanLab (University of
Aberdeen) and NIOZ (Royal
Netherlands Institute of Sea
Research) (from CoralFISH
Gallery); (i) Photo © and
courtesy of OceanLab
(University of Aberdeen)
(from CoralFISH Gallery)
344 G. D’Onghia
In fact, areas with damaged H. willemoesi had far fewer indi- The most abundant scorpaenid fish were S. alascanus and the
viduals and areas without sea whips had no individuals. In rockfish Sebastes spp., mostly S. zacentrus. Thornyhead
addition, other fishes were occasionally seen within the sea abundance did not vary with substratum type while rockfish
whip habitat, including arrow tooth flounders (Atheresthes abundance increased significantly with higher substratum
stomias), saw back poachers (Sarritor frenatus) and big and epifauna relief. Over 50% of Primnoa pacifica taller
skate (Beringraja binoculata), but none seemed to be as con- than 30 cm had at least one associated rockfish and often sev-
sistently associated with this habitat as the rockfish (Brodeur eral while, in comparison, no rockfish were observed with P.
2001). Successively, Miller et al. (2012) reported that rock- pacifica under 30 cm in height.
fishes, including S. alutus, preferentially utilise corals for Association of fish with sponges, black corals and gorgo-
habitat in Pribilof Canyon. nians was also examined, using submersible, in continental
Using submersible, six species of rockfish (rougheye shelf and slope ecosystems off southern California (Tissot
rockfish Sebastes aleutianus, redbanded rockfish S. bab- et al. 2006). Six species were found at significantly higher
cocki, shortraker rockfish S. borealis, sharpchin rockfish S. frequencies than predicted by their density along transects:
zacentrus, dusky rockfish S. ciliatus and yelloweye rockfish cowcod (Sebastes levis), bank rockfish (Sebastes rufus),
S. ruberrimus) were found associated with Primnoa in the swordspine rockfish (Sebastes ensifer), shortbelly rockfish
Gulf of Alaska (Krieger and Wing 2002). These fishes have (Sebastes jordani), pinkrose rockfish (Sebastes simulator),
been considered as protection seekers and were observed and members of the rockfish subgenus Sebastomus. Tissot
either beneath, among or above the corals. Shrimps were not et al. (2006) concluded that there is not necessarily a func-
identified, but hundreds of them were observed among the tional relationship between these groups of organisms.
branches of large colonies. Krieger and Wing (2002) sug- However, the authors also recognised the relatively low num-
gested that the large rockfish (S. borealis and S. aleutianus) ber and size of individual sponges, black corals and gorgoni-
associate with corals for feeding since shrimps are their main ans observed in their study.
prey. Off Alaska, the rockfish, Sebastes spp. and the short-
spine thornyhead (Sebastolobus alascanus), and Atka mack- 30.3.1.5 Central Pacific
erel (Pleurogrammus monopterygius) were among the most A study carried out in the north-western Hawaiian Islands
common fish captured with gorgonians (Callogorgia, with submersibles revealed that the deep-sea coral colonies
Primnoa, Paragorgia, Thouarella and Arthrogorgia), cup may aggregate individuals of C. oceanicus and attract foraging
corals (Caryophyllia sp.) and hydrocorals, whereas flatfish monk seals to Gerardia sp. and Corallium sp. reefs at depths
(Bothidae and Pleuronectidae) and gadids (mostly the Alaska over 500 m (Parrish et al. 2000). Notably, the seals searched
pollock Gadus chalcogrammus) and the Pacific cod (Gadus for prey in low-relief bottom habitat. This uniform habitat was
macrocephalus) were the most common species associated probably selected over the complex coral reef habitat in rela-
with the soft coral Gersemia sp. (Heifetz 2002). Roberts tion to the differences in accessibility of prey. In fact, fish spe-
et al. (2006) reported photos of rockfish (Sebastes sp.) among cies of the coral reef use available shelter to avoid predators
gorgonian corals (Primnoa sp.) in the Gulf of Alaska. while the foraging technique of the seal is best suited for uni-
Stone (2006) observed many species exhibiting a strong form habitats where the amount of territory covered can be
association with corals and emergent epifauna in the Aleutian maximised. Exploiting a much higher probability of capture in
Islands of Alaska. Habitats that had the highest densities of an area of lower prey density on the deep slope may yield
corals also supported the highest densities of several commer- more than a low probability of capture at high prey densities in
cial species. The association with emergent epifauna ranged the coral shallows (Parrish et al. 2000). This is a clear case
from 100% for prowfish (Zaprora silenus), followed by sharp- study of a refuge effect of coral habitat for a fish species.
chin rockfish (S. zacentrus), rockfish juveniles (97%), rough-
eye rockfish (S. aleutianus), dusky rockfish (S. ciliates),
northern rockfish (S. polyspinis), Pacific ocean perch (S. alu- 30.3.2 CWC as Spawning and Nursery Habitats
tus), shortraker rockfish (S. borealis), “other” rockfish
(Sebastes spp.), skate (Rajidae), Pacific cod, sculpins, Atka 30.3.2.1 Northeast Atlantic
mackerel, shortspine thornyhead (S. alascanus), giant grena- Lophelia reefs in Norwegian waters were observed to support
dier (Albatrossia pectoralis), up to 31% in righteye flounders dense aggregations of Sebastes spp. which in May-June were
(Pleuronectidae), indicating that these habitats appear to be dominated by gravid females with distended bellies, indicat-
more frequently used within the region (Stone 2006). ing that CWCs may play a role in the reproductive cycle of
In situ images were used to examine which variables of redfish species and that both spawning females and juveniles
the seafloor, including epifauna cover, might influence scor- can find protection from predators in the coral h abitat (Furevik
paenid fish abundance patterns on Learmonth Bank off et al. 1999, in Fosså et al. 2002). The small specimen of S.
northern British Columbia (Du Preez and Tunnicliffe 2011). viviparus trapped in a coral block recovered from L. pertusa
reefs on the Faroe shelf might be considered as a first proof of the catshark nursery area is substrate-specific, taxon-specific
juveniles in coral habitat (Jensen and Frederiksen 1992). or site-specific (Etnoyer and Warrenchuk 2007). Living eggs
Costello et al. (2005) hypothesised that Lophelia reefs of an unidentified Liparidae fish were collected and observed
conceal juveniles and thus they might act as a nursery habitat. in the octocorals Anthothela sp. and Acanthogorgia sp. from
These authors observed the presence of gravid redfish (S. the U.S. middle Atlantic slope (Ross et al. 2015).
viviparus) as well as egg cases of skates (Raja sp.) at Sula Specimens of the Pluto skate Fenestraja plutonia were col-
Ridge indicating that the reefs are also spawning sites for lected using otter trawl off North Carolina; three egg-bearing
some fish species. More recently, the occurrence of some females, newly hatched juveniles and deposited egg cases
gravid individuals of Sebastes sp. (mainly S. viviparus) was were collected near the Cape Lookout deep coral banks
reported associated with the CWC reef at Rockall Bank (Quattrini et al. 2009). These data and those of Ross and
(Milligan et al. 2016). On the Mingulay Reef Complex, video Quattrini (2007), who observed this fish near deep coral banks
surveys revealed spawning grounds of G. melastomus (Henry off the south-eastern U.S., suggested that Lophelia coral bank
et al. 2013). Shark egg cases were always found nested in live area off Cape Lookout represents an important egg-laying area
corals at a narrow depth range (165–172 m) on slightly and possibly a nursery area for this skate species.
inclined sites colonised by live corals. Henry et al. (2013) Fish larvae, mainly belonging to the Acadian redfish
suggested that G. melastomus targets coral colonies because Sebastes fasciatus and beaked redfish Sebastes mentella,
of multiple benefits. The hard colonial skeleton of Lophelia were found on deep-water sea pens (mostly Anthoptilum
provides a framework of branches that could deter egg preda- grandiflorum, Pennatula aculeata, Halipteris finmarchica)
tors while reducing the risk of eggs drifting away. A coral by Baillon et al. (2012, 2014). The closeness of the associa-
framework also elevates capsules into water currents that ven- tion between these fish and CWCs suggests that the vivipa-
tilate the eggs, with coral polyps helping to remove sediments rous redfish release their progeny near corals, where they
that could otherwise accumulate and smother the egg cases. remain during early ontogeny. It seems that the calcified
parts (sclerites) and/or toxic chemicals produced by soft cor-
30.3.2.2 Northwest Atlantic als deter potential predators. Therefore, fish may release lar-
Using a submersible, Reed and Gilmore (1981) observed a vae among corals to provide them with shelter and protection.
male and a female of rough tail stingray, Dasyatis centroura, The number of fish larvae harboured was positively corre-
in an apparent courtship or mating ritual near the base of a lated to the size of the sea pen colony. Eggs or larvae of the
coral bank of O. varicosa at a depth of 80 m, off central east- lantern fish (Benthosema glaciale) and the eelpout (Lycodes
ern Florida. Successively, schools of thousands of small indi- esmarkii) were also found (Baillon et al. 2012, 2014). Buhl-
viduals of B. vivanus swimming among the branches of O. Mortensen et al. (2017a) reported a figure of a colony of P.
varicosa were observed (Reed 1985 and Reed and Hoskin arborea with 26 eggs of deep-sea catshark (Apristurus pro-
(1987), in Reed 2002). Moreover, Oculina reefs were fundorum) collected with bottom trawl at around 500 m
observed as breeding grounds for commercially important depth in the northeast Channel, Nova Scotia.
populations of M. microlepis, M. phenax, C. striata, H. nive-
atus and E. drummondhayi as well as nursery grounds for H. 30.3.2.3 Northeast Pacific
niveatus and E. drummondhayi (Gilmore and Jones 1992; In situ evidence of habitat functions for deep-sea corals was
Coleman et al. 1996; Koenig et al. 2000; Reed 2002; Koenig derived from video and photographic observations (e.g. an
et al. 2005; Reed et al. 2005). egg case attached to a Paragorgia) (Etnoyer and Morgan
Castro et al. (1998) collected two egg cases of the chain 2005). Evidence of egg masses of the goldeneye snailfish
catshark S. retifer attached to corals accidentally entangled Allocareproctus unangas found deposited surrounding stalks
in long line used in rough bottom areas off South Carolina, at of the octocoral Primnoa sp. from the Aleutian Islands was
depths of 230–450 m. Another egg case attached to a coral provided by Busby et al. (2006). These eggs contained
was obtained by submersible at 240 m depth in the Gulf of embryos in the flexion stage of development. Another stalk
Mexico (Castro et al. 1998). In this geographic area, Etnoyer of Primnoa sp. collected in the same area had three attached
and Warrenchuk (2007), using an ROV, recorded 296 egg masses of eggs belonging to other unidentified Liparidae
cases attached to 117 colonies of Callogorgia americana fishes (Busby et al. 2006).
delta with a maximum of 17 cases observed on a single col- The egg cases of the brown catshark Apristurus brunneus
ony. The egg cases were suggested to be of the chain catshark were observed attached to filter-feeding invertebrates such as
S. retifer, but they belong to another species (Ross et al. gorgonians (e.g. Euplexaura marki), sponges and anemones,
2015). However, this occurrence demonstrated that large while those of the filetail catshark Parmaturus xaniurus were
monotypic fields of gorgonian octocorals on low relief found attached by their long tendrils to substrates, such as
mounds can provide a nursery area for fish species in the corals (e.g. Antipathes sp.), hydroids, ascidians and other
Gulf of Mexico, although it was insufficient to define whether egg cases (Flammang et al. 2007, 2011).
346 G. D’Onghia
30.3.2.4 Southeast Pacific Other fishing gears, such as longlines, gillnets, pots and
Concha et al. (2010) collected eighteen capsules from nine traps, can also cause impact to CWC communities since they
gravid females of the dusky catshark Bythaelurus canescens cause breakage of the coral colonies from rocks and boulders
and four capsules were attached to the deep-sea coral (e.g. Butler 2005; Reed et al. 2005; Morgan et al. 2005; Stone
Antipathes speciosa. All females and corals were caught off 2006; Lumsden et al. 2007; Mortensen et al. 2008; Hourigan
southern Chile as by-catch of bottom longline fisheries. 2009; Durán-Muñoz et al. 2011; D’Onghia et al. 2012;
Sampaio et al. 2012; Pham et al. 2014; Hinz 2017). Longlining
is often used in deep waters with hard untrawlable substrates
30.4 Fishing Impact to Cold-Water Coral that can be suitable habitats for CWCs, which increases the
Habitats probability of coral by-catch. Disturbance caused by long-
lines is not well defined and can be easily masked by natural
The CWC habitats are considered valuable fishing areas due events or disturbance created by other gear types (Heifetz
to the distribution and abundance of fish species of commer- et al. 2009; Hourigan 2009; Sampaio et al. 2012). Longlines,
cial interest (e.g. Fosså et al. 2002; Morgan et al. 2005; Reed gillnets, pots and traps can also cause: (i) “ghost fishing”,
et al. 2005; D’Onghia et al. 2017; Hinz 2017). The impact of since discarded or lost gear may continue to catch different
fishing to CWC communities has been documented both in organisms for a long time; (ii) mechanical injuries on benthic
the Atlantic and Pacific Oceans in relation to the exhaustion species if drifting on the sea floor; (iii) accumulation of debris
of commercial fish stocks in readily accessible inshore on the bottoms from lost gear, altering habitats (e.g. Reed
waters (e.g. Rogers 1999; Koenig et al. 2000; Roberts et al. et al. 2005; Matsuoka et al. 2005; Brown and Macfadyen
2000; Duncan 2001; Fosså et al. 2002; Grehan et al. 2005; 2007; Bo et al. 2014a; Hinz 2017).
Mortensen et al. 2005; Reed et al. 2005; Wheeler et al. Other indirect effects of the different fishing gears include
2005b; Stone 2006; Hourigan et al. 2007; Lumsden et al. increased vulnerability to epibiosis, parasitism and preda-
2007; Hourigan 2009; Durán-Muñoz et al. 2011; Sampaio tion, especially for corals damaged and detached from the
et al. 2012; Pham et al. 2014). seafloor, as well as interruption of reproduction in damaged
Although different types of fishing gears impact the sea- corals due to a reallocation of energy reserves for tissue
floor and pose potential threats to CWC communities, otter repair and regeneration (e.g. Mortensen et al. 2005; Stone
trawls and dredges are the most destructive gears (e.g. Hall- and Shotwell 2007; Bo et al. 2009).
Spencer et al. 2002; Roberts 2002; Morgan et al. 2005;
Lumsden et al. 2007; Hourigan 2009; Pham et al. 2014; Hinz
2017). The main impact of trawling and dredging on CWC 30.4.1 Mediterranean Observations
habitats is the mechanical damage caused by otter boards,
nets and iron/steel structures that destroy the three- The Mediterranean CWC communities are subject to fishing
dimensional (3D) coral colonies and reduce habitat com- impacts (e.g. Orejas et al. 2009; Maynou and Cartes 2011;
plexity that provide shelter for fishes and invertebrates (Hinz Bo et al. 2011b, 2012, 2014a; Madurell et al. 2012; Cartes
2017 and references therein). The impacts of bottom trawl- et al. 2013; Fabri et al. 2014; Mytilineou et al. 2014; Savini
ing on the benthos have been compared to clear-cutting tech- et al. 2014; D’Onghia et al. 2017; Mastrototaro et al. 2017;
niques in old growth forests (Watling and Norse 1998). The Taviani et al. 2017; Otero and Marin, this volume).
morphology of the upper continental slope could be altered Explorations in the SML CWC province have provided
and the habitat complexity could be markedly reduced by images of trawling traces, fishing line remains and solid waste
intensive bottom trawling, producing comparable effects on in the coral community (Taviani et al. 2005; Freiwald et al.
the deep sea floor to those generated by agricultural plough- 2009; Vertino et al. 2010). Savini et al. (2014) recorded lost or
ing on land (Puig et al. 2012). discarded long lines and nets in association with coral rubble,
Since trawling and dredging can often be carried out on boulder fields and loosely packed coral habitats. These
muddy bottoms near to coral areas, they have an indirect authors identified trawling traces within mud-dominated sed-
impact due to the alterations of the hydrodynamic and sedi- iments in the vicinity or at the base of coral mounds or in
mentary conditions (e.g. Piskaln et al. 1998; Watling and between coral mounds. More recently, D’Onghia et al. (2017),
Norse 1998; Purser 2015). In addition, an increase in sedi- using towed cameras, observed remains of long lines on the
ment suspension from trawling activities could affect corals bottoms and/or entangled in c orals as well as trawl door scars
and associated benthic species in neighbouring coral mounds. on the sea floor around the coral mounds in the Fisheries
In fact, coral species, like all suspension feeders, are particu- Restricted Area (FRA), within the SML CWC province.
larly vulnerable to the effects of increased sedimentation These authors also examined the geographic distribution of
(e.g. Rogers 1999; Buhl-Mortensen et al. 2010; Purser 2015). fishing effort through an observers’ program of longline and
trawl fishing activities during 2009 and 2010 and Vessel
Monitoring by satellite System (VMS) data from 2008 to (Tuscan Archipelago, Tyrrhenian Sea) where Eunicella cav-
2013. The longliners mainly fished on the shelf in the north of olinii and Parantipathes larix were clearly entangled in lost
the SML CWC province and off the FRA whereas the trawl- lines (Bo et al. 2014b). The area of the Marco Bank (north-
ers generally fished on the muddy bottoms of the upper and west coasts of Sicily, south Tyrrhenian Sea) appeared
middle slope within the SML CWC province as well as near strongly affected by fishing activities mainly focused on the
and inside the northward limit of the FRA. These results indi- blackspot seabream Pagellus bogaraveo. Ghost longlines
cate a greater impact of trawling than longlining and that con- were present everywhere entangled in the branches of the
servation and effective management of this vulnerable marine largest coral colonies of Leiopathes glaberrima and C. verti-
ecosystems (VMEs) (FAO 2009) remain difficult. Coral by- cillata, this latter severely damaged by lost lines (Bo et al.
catch was observed in the Ionian (Vafidis et al. 2006; 2014c). Lost longlines and lines entangled in the colonies of
Mytilineou et al. 2014; D’Onghia et al. 2017) and along the these two species were also observed on a rocky bank off the
southern Adriatic Sea (D’Onghia et al. 2016). southwest coasts of Sardinia (western Mediterranean) (Bo
A total of 197 bottom longlines were recorded in the Cap de et al. 2015).
Creus canyon (western Mediterranean) (Orejas et al. 2009).
Although the statistical analysis related to this finding did not
show a clear pattern in the relationship between benthic long- 30.5 Discussion and Conclusions
line distribution on the seabed and coral density, coral occur-
rence correlated with bottom longlines in two video transects. 30.5.1 Ecological Interactions
The large quantity of benthic longlines found within this can-
yon indicates that the seabed is periodically exposed to drag- Most studies examined in this review show that the CWC
ging lines (Orejas et al. 2009). The seafloor disturbance due to habitats are important habitats for fish species. Greater abun-
trawling on soft bottoms and to longlines on rocky substrates dance and positive effects related to CWCs have been
was also recorded in the Gulf of Lion (Fabri et al. 2014). The detected in many fish species both throughout the
colonies of scleractinian corals (Lophelia pertusa and Mediterranean and world’s oceans. With this regard, several
Madrepora oculata) were often observed entangled in fishing authors suggested that CWCs can be functionally equivalent
lines in both the Lacaze-Duthiers and Cassidaigne canyons. to other hard-bottom structurally complex habitats and that
The alcyonacean Callogorgia verticillata was also severely the association with CWCs varies largely according to the
affected by bottom fishing gears since many colonies were different coral and fish species, depth, time of the year and
entangled in bottom lines and fishing nets. The high diversity spatial scale (e.g. Auster et al. 2005; Stone 2006; Harter et al.
sheltered by the structure-forming gorgonians is attractive for 2009; Ross and Quattrini 2009; Du Preez and Tunnicliffe
local fisheries even if the examined area is located far from the 2011; D’Onghia et al. 2012; Quattrini et al. 2012; Biber et al.
coast (60 km). Lost fishing gears, lead weights and ropes, dam- 2014; Kutti et al. 2015; Milligan et al. 2016; Linley et al.
aging structure-forming fauna and breaking cnidarian colonies 2017). However, several studies have provided evidence of
were observed in most canyons off the French coast (Fabri the role of CWCs as critical habitats for fish since:
et al. 2014). Recently, discarded fishing gears, including entan-
gled nets and lines, have been observed in the Sardinian 1. Several species have been observed and suggested to ben-
Madrepora CWC province (western Mediterranean) (Taviani efit from shelter and productive feeding in the complex
et al. 2017). Longline and trawling impacts have also been heterogeneous habitats built by corals (e.g. Mortensen
observed on Isidella elongata facies in Balearic Sea, including et al. 1995; Brodeur 2001; Fosså et al. 2002; Husebo et al.
a canyon southwest of Formentera (Mastrototaro et al. 2017). 2002; Krieger and Wing 2002; Jonsson et al. 2004;
The occurrence of lost fishing gears, anchor and rope, Costello et al. 2005; Sulak et al. 2007; Buhl-Mortensen
entangled and damaged colonies of different species, et al. 2010; D’Onghia et al. 2010, 2011, 2012; Quattrini
together with a significant degradation of the habitat and the et al. 2012; Biber et al. 2014; Kutti et al. 2014; Gomes-
communities, were recorded in several rocky areas in the Pereira et al. 2017) (Table 30.1);
southern Tyrrhenian Sea (Bo et al. 2011a, 2012, 2014a). The 2. A variety of cartilaginous and teleost fishes use CWC
majority of the debris was due to longlines, for which a sig- habitats for reproduction and as nursery areas (e.g. Reed
nificant inverse relationship between the presence of these and Gilmore 1981; Gilmore and Jones 1992; Koenig et al.
lost gears and the distance from the coast was detected. Other 2000; Fosså et al. 2002; Reed 2002; Etnoyer and Morgan
obvious factors, such as the depth of the site, topography and 2005; Busby et al. 2006; Stone 2006; Etnoyer and
the occurrence of commercial target stocks may influence Warrenchuk 2007; Quattrini et al. 2009; Concha et al.
the fishing effort and, in turn, the impact on benthic commu- 2010; D’Onghia et al. 2010, 2016; Flammang et al. 2011;
nities (Bo et al. 2014a). Lost nets and longlines were observed Baillon et al. 2012; Henry et al. 2013; Bo et al. 2015; Cau
on rocky shoals located southeast of the Island of Montecristo et al. 2017; Mastrototaro et al. 2017) (Table 30.2).
348 G. D’Onghia
Table 30.1 Most common fish species observed and suggested to use cold-water coral (CWC) habitats for shelter and/or feeding
Geographic area CWC species Fish species Authors
Mediterranean Sea Madrepora oculata, Cartilaginous fish: Etmopterus spinax. Hebbeln et al. (2009), D’Onghia
Lophelia pertusa (with Galeus melastomus, Scyliorhinus canicula et al. (2010, 2011, 2012),
presence of other CWCs) Teleost fish: Coelorinchus caelorhincus, Capezzuto et al. (2012), Sion et al.
Conger conger, Helicolenus dactylopterus, (2012), Maiorano et al. (2013),
Hoplostethus mediterraneus, Merluccius Carluccio et al. (2014), D’Onghia
merluccius, Micromesistius poutassou, Phycis et al. (2016), and Linley et al.
blennoides, Pagellus bogaraveo, Polyprion (2017)
americanus
Mediterranean Sea Leiopathes glaberrima, Cartilaginous fish: G. melastomus, E. spinax Mytilineou et al. (2014), Angeletti
Isidella elongata Teleost fish: Benthocometes robustus, H. et al. (2015), and Mastrototaro
dactylopterus, H. mediterraneus, et al. (2017)
Lepidorhombus boscii, M. merluccius, M.
poutassou, P. americanus, P. blennoides
Mediterranean Sea Gorgonians (mostly Cartilaginous fish: Scyliorhinus canicula, S. Bo et al. (2011a, 2012, 2014b),
Callogorgia verticillata) stellaris Fabri et al. (2014), Bo et al.
and antipatharians (mostly Teleost fish: Anthias anthias, B. robustus, (2015), and Cau et al. (2017)
Leiopathes glaberrima, Capros aper, Cepola macrophthalma, H.
Antipathes dichotoma, dactylopterus, Lappanella fasciata,
Parantipathes larix) Macroramphosus scolopax, Phycis phycis,
Zeus faber
Northeast Atlantic Lophelia pertusa Cartilaginous fish: Galeus melastomus Jensen and Frederiksen (1992),
(Faroe shelf, Norwegian Teleost fish: Anarhichas lupus, Brosme Mortensen et al. (1995), Furevik
and Swedish waters) brosme, Gadus morhua, Lycodes vahli, Molva et al. (1999) in Fosså et al. (2002),
molva, Pollachius virens, Sebastes viviparus, Freiwald et al. (2002), Husebo
Sebastes marinus, Trisopterus minutus et al. (2002), Jonsson et al. (2004),
Costello et al. (2005), Roberts
et al. (2005), Kutti et al. (2014,
2015), and Linley et al. (2017)
Northeast Atlantic Lophelia pertusa (some Cartilaginous fish: Galeus melastomus, Costello et al. (2005), Wheeler
(from Faroe-Shetland studies with presence of Hexanchus griseus, Scyliorhinus canicula et al. (2005a), Roberts et al.
Channel to Porcupine Madrepora oculata, black Teleost fish: Benthocometes robustus, Brosme (2008), Durán-Muñoz et al. (2009),
Seabight, Bay of Biscay corals, octocorals and brosme, Guttigadus latifrons, Helicolenus Söffker et al. (2011), Henry et al.
and Azores) hydrocorals) dactylopterus, Lappanella fasciata, Lepidion (2013), Biber et al. (2014),
eques, Molva molva, Mora moro, Neocyttus Milligan et al. (2016), Gomes-
helgae, Phycis blennoides, Sebastes viviparus Pereira et al. (2017), Lavaleye
et al. (2017), Linley et al. (2017)
Northwest Atlantic Oculina varicosa Teleost fish: Baldwinella vivanus, Reed (2002), Reed et al. (2005),
(south-eastern United Centropristis striata, Epinephelus Reed and Ross (2005), and Harter
States, eastern Florida) drummondhayi, E. itajara, E. morio, et al. (2009)
Hyporthodus niveatus, H. nigritus, Lutjanus
campechanus, L. griseus, Mycteroperca
microlepis, M. phenax
Northwest Atlantic Lophelia pertusa (some Cartilaginous fish: Scyliorhinus retifer Wenner and Baran (2001) in Reed
(south-eastern United studies with presence of Teleost fish: Anthias woodsi, Beryx et al. (2006); Reed and Ross
States, eastern Florida, other CWCs) decadactylus, Conger oceanicus, Dysommina (2005), Reed et al. (2006), Sulak
Gulf of Mexico) rugosa, Eptatretus lopheliae, Gephyroberyx et al. (2007), Ross and Quattrini
darwini, Grammicolepis brachiusculus, (2007, 2009), Fernholm and
Helicolenus dactylopterus, Hoplostethus Quattrini (2008), and Quattrini
occidentalis, Hyperoglyphe perciformis, et al. (2012)
Hyporthodus niveatus, Idiastion kyphos,
Laemonema barbatulum, L. melanurum, L.
goodebeanorum, Nezumia sclerorhynchus,
Polyprion americanus, Trachyscorpia
cristulata
Central eastern Lophelia pertusa Teleost fish: Gephyroberyx darwini, Le Guilloux et al. (2009) and
Atlantic Helicolenus dactylopterus, Malacocephalus Buhl-Mortensen et al. (2017b)
occidentalis, Nettastoma melanorum
Northeast Pacific (Gulf Sea whips, Halipteris Teleost fish: Sebastes alutus Krieger (1993), Brodeur (2001)
of Alaska, Bering Sea) willemoesi and Miller et al. (2012)
(continued)
Northeast Pacific (Gulf Primnoa spp., Callogorgia Teleost fish: Albatrossia pectoralis, Gadus Heifetz (2002), Krieger and Wing
of Alaska, Aleutian sp., Gersemia sp., other chalcogrammus, G. macrocephalus, Sebastes (2002), Roberts et al. (2006), Stone
Islands, British gorgonians, black corals, aleutianus, S. alutus, S. babcocki, S. borealis, (2006), Tissot et al. (2006), and Du
Columbia, off sea pens, hydrocorals and S. ciliatus, S. ensifer, S. jordani, S. levis, S. Preez and Tunnicliffe (2011)
California) other epifauna polyspinis, S. ruberrimus, S. rufus, S.
simulator, S. zacentrus, Sebastolobus
alascanus, Pleurogrammus monopterygius,
Zaprora silenus
Central Pacific Gerardia sp., Corallium sp. Teleost fish: Conger oceanicus Parrish et al. (2000)
Table 30.2 Fish species observed to use cold-water coral (CWC) habitats for spawning and/or nursery
Mediterranean Sea Madrepora oculata, Lophelia Cartilaginous fish: Etmopterus D’Onghia et al. (2010, 2016)
pertusa (with presence of other spinax, Galeus melastomus
CWCs) Teleost fish: Conger conger,
Helicolenus dactylopterus,
Merluccius merluccius,
Micromesistius poutassou, Pagellus
bogaraveo, Phycis blennoides
Mediterranean Sea Leiopathes glaberrima Cartilaginous fish: Scyliorhinus Hebbeln et al. (2009), Bo et al.
canicula (2015), and Cau et al. (2017)
Mediterranean Sea Isidella elongata Cartilaginous fish: Scyliorhinus sp. D’Onghia (this chapter, ref.
Mastrototaro et al. 2017)
Northeast Atlantic (from Lophelia pertusa Cartilaginous fish: Galeus Jensen and Frederiksen (1992),
Norwegian waters to melastomus Furevik et al. (1999) in Fosså et al.
Rockall Bank) Teleost fish: Sebastes viviparus (2002), Costello et al. (2005), Henry
et al. (2013), and Milligan et al.
(2016)
Northwest Atlantic Oculina varicosa (and other Cartilaginous fish: Dasyatis Reed and Gilmore (1981), Gilmore
(south-eastern United deep-water corals) centroura, Scyliorhinus retifer and Jones (1992), Coleman et al.
States, eastern Florida, Teleost fish: Baldwinella vivanus, (1996), Castro et al. (1998), Koenig
Gulf of Mexico) Mycteroperca microlepis, M. phenax, et al. (2000), (2005), Reed (2002),
Centropristis striata, Hyporthodus and Reed et al. (2005)
niveatus, Epinephelus drummondhayi
Northwest Atlantic (Gulf Callogorgia americana delta Cartilaginous fish: Scyliorhinus Etnoyer and Warrenchuk (2007)
of Mexico) retifer (confuted by Ross et al. 2015)
Northwest Atlantic (off Lophelia pertusa Cartilaginous fish: Fenestraja Ross and Quattrini (2007) and
north Carolina) plutonia Quattrini et al. (2009)
Northwest Atlantic (off Paragorgia arborea, deep- Cartilaginous fish: Apristurus Baillon et al. (2012, 2014) and
eastern Canada, Nova water sea pens (mostly profundorum Buhl-Mortensen et al. (2017a)
Scotia) Anthoptilum grandiflorum, Teleost fish: Benthosema glaciale,
Pennatula aculeata, Halipteris Lycodes esmarkii, Sebastes fasciatus,
finmarchica) S. mentella
Northeast Pacific Primnoa sp. Teleost fish: Allocareproctus Busby et al. (2006)
(Aleutian Islands) unangas
Northeast Pacific (from Gorgonians (e.g. Euplexaura Cartilaginous fish: Apristurus Flammang et al. (2007, 2011)
Washington to California) marki), black corals (e.g. brunneus, Parmaturus xaniurus
Antipathes sp.), hydroids
Southeast Pacific (off Antipathes speciosa Cartilaginous fish: Bythaelurus Concha et al. (2010)
southern Chile) canescens
With regard to the first point, the 3D CWC framework can cal filter that intercept and trap organic matter from the water
provide habitats not present in the surrounding areas and column and can be a hot spot of zooplankton, macrofaunal
firm substrates within extended areas of soft homogeneous biomass and carbon cycling along continental margins (Van
bottoms. The topography and hydrography of the sites where Oevelen et al. 2009; Mienis et al. 2014; Soetaert et al. 2016;
corals thrive can favour a greater food supply for the corals Buhl-Mortensen et al. 2017a). Several works report enhanced
themselves and the associated fauna. CWCs act as a biologi- density of zooplankton as potential prey for planktivorous
350 G. D’Onghia
fish and high density of invertebrates between and around melastomus, S. canicula) (e.g. Mortensen et al. 1995; Koenig
corals as potential food for benthos feeders and scavengers et al. 2000; Fosså et al. 2002; Husebo et al. 2002; Krieger
(e.g. Reed et al. 1982; Mortensen et al. 1995; Husebo et al. and Wing 2002; Costello et al. 2005; Koenig et al. 2005;
2002; Costello et al. 2005; Sulak et al. 2007; D’Onghia et al. Etnoyer and Warrenchuk 2007; Ross and Quattrini 2007;
2011; Biber et al. 2014). In addition, fishes may use CWC D’Onghia et al. 2010, 2011, 2016; Du Preez and Tunnicliffe
habitats as refuges to maintain position in an optimal feeding 2011; Baillon et al. 2012; Quattrini et al. 2012; Henry et al.
location, reducing the metabolic cost of actively swimming 2013; Bo et al. 2015; Cau et al. 2017).
in strong currents between feeding periods (Mortensen et al. Some fish species (i.e. those of the Scyliorhinidae,
2005; Quattrini et al. 2012). The high biodiversity associated Sebastidae, Serranidae, Berycidae, Zoarcidae, Lotidae,
with CWCs attract fishes with different feeding strategies Moridae, Congridae and Liparidae families) seem to be more
and behaviours (e.g. Buhl-Mortensen and Mortensen 2004a, tightly associated to CWC habitats. However, from the avail-
b, c, 2005; Lumsden et al. 2007; Edinger et al. 2007; Sulak able knowledge, they cannot be considered as habitat spe-
et al. 2007; Buhl-Mortensen et al. 2010 and references cialists. In fact, most of these species (e.g. Sebastes spp., H.
therein; D’Onghia et al. 2011; Quattrini et al. 2012; Girard dactylopterus, B. decadactylus, C. oceanicus, C. conger, P.
et al. 2016). The 3D CWC structure may function in a very bogaraveo, G. melastomus), which obtain benefits from
similar way to their tropical counterparts, providing feeding CWC habitats, could be facultative inhabitants since they
sites for aggregating fish species, hiding places from preda- have also been found in other types of habitats (e.g. Uiblein
tors and ambush sites for predators (e.g. Hourigan et al. et al. 2003; Reed et al. 2006; Ross and Quattrini 2007;
2007). Most tropical reef fish do not have an obligate rela- Roberts et al. 2008; D’Onghia et al. 2012, 2016; Quattrini
tionship with individual coral species, but they do depend on et al. 2012; Biber et al. 2014; Kutti et al. 2014; Milligan et al.
the reef environment (Sale 2002). 2016). In this respect, species that display ontogenetic migra-
With regard to the second topic (spawning and nursery), tion as well as those that cover larger areas during foraging
particular case studies and observations reported here reveal activity, may visit both coral and non coral habitats. For
a clear, probably obligate, relationship between fishes and example, H. dactylopterus and P. bogaraveo generally show
corals (Castro et al. 1998; Busby et al. 2006; Etnoyer and ontogenetic migration, with juveniles distributed in the shal-
Warrenchuk 2007; Concha et al. 2010; Flammang et al. lower waters on muddy bottoms and adults at greater depths
2011; Baillon et al. 2012, 2014; Henry et al. 2013; Bo et al. often containing CWCs, outcrops, banks and habitats less
2015; Cau et al. 2017). In addition, some deep-sea skates and accessible to trawling (Uiblein et al. 2003; Reed et al. 2006;
rays are not tightly associated with corals (Costello et al. Ross and Quattrini 2007; Roberts et al. 2008; D’Onghia
2005; Ross and Quattrini 2007; Sulak et al. 2007), but their et al. 2010, 2016; Mytilineou et al. 2013; Milligan et al.
egg cases co-occur with these benthic organisms (e.g. 2016); G. melastomus is a very mobile shark which swims
Costello et al. 2005; Etnoyer and Morgan 2005; Quattrini over different habitats searching for food based on benthic
et al. 2009; Buhl-Mortensen et al. 2017a), suggesting crustaceans, among which Munida sp., and a mixture of ben-
changes in habitat use over time and CWCs as an important thopelagic and mesopelagic species (euphausiids, Pasiphaea
habitat for reproduction and for the early life stages. CWCs multidentata, fishes and cephalopods) (e.g. Carrassón et al.
also seem to be used by a variety of teleost fishes, such as 1992; Roberts et al. 2008; Durán- Muñoz et al. 2009;
Sebastes spp. (Fosså et al. 2002; Costello et al. 2005; Milligan D’Onghia et al. 2012; Kutti et al. 2014; Mastrototaro et al.
et al. 2016), Mycteroperca microlepis, M. phenax, 2017). Contrary to all these facultative inhabitants, Eptatretus
Centropristis striata, Hyporthodus niveatus and Epinephelus lopheliae, which was videotaped and caught in close associ-
drummondhayi (Gilmore and Jones 1992; Coleman et al. ation with a Lophelia reef habitat (Fernholm and Quattrini
1996; Koenig et al. 2000; Reed 2002; Koenig et al. 2005; 2008), might be a specialist inhabitant, but also in this case
Reed et al. 2005), Galeus melastomus, Conger conger, the knowledge is very scant.
Helicolenus dactylopterus, Merluccius merluccius, Phycis Based on a variety of studies, a consensus has emerged
blennoides, Pagellus bogaraveo (D’Onghia et al. 2010, that environmental variables, such as physical structures,
2016) since adult reproductive individuals were often food availability, predator occurrence, depth, current speed
reported associated with the coral habitats. and temperature, can all influence the distribution of the spe-
The papers examined in this review show that the poten- cies and their association with CWCs (e.g. Harter et al. 2009;
tial benefits provided by CWCs for several fish species are Buhl-Mortensen et al. 2010; Du Preez and Tunnicliffe 2011;
not only related to food supply, but concurrently as spawning Söffker et al. 2011; Quattrini et al. 2012; Biber et al. 2014;
sites, nursery grounds, and protection refuges from preda- Milligan et al. 2016; Buhl-Mortensen et al. 2017a; Henry
tors, bottom currents and fishing activities (e.g. Sebastes and Roberts 2017). Often the potential importance of CWCs
spp., Mycteroperca spp., Conger oceanicus, C. conger, B. remains unclear because studies do not coincide with the
brosme, H. dactylopterus, P. bogaraveo, B. decadactylus, G. period when fish might use this habitat (e.g. Auster 2007;
Baillon et al. 2012; Milligan et al. 2016; Linley et al. 2017). conducted in the Mediterranean, but longlining and trawling
Moreover, there are currently many methodological difficul- as well as lost fishing gears are among the major causes of
ties in sampling deep-sea species and studying coral- degradation of CWC habitats in the Mediterranean (e.g. Bo
associated fish density and diversity that need to be addressed et al. 2014a; Savini et al. 2014; D’Onghia et al. 2017; Taviani
and improved (e.g. Ross and Quattrini 2007; Roberts et al. et al. 2017).
2009; Buhl-Mortensen et al. 2010; Milligan et al. 2016). Despite this evidence and the different conservation ini-
Despite these uncertainties and difficulties, from all the tiatives proposed for the Mediterranean CWCs (e.g. de Juan
above reported, there are several sources of evidence that and Lleonart 2010; Oceana 2011; Micheli et al. 2013; Otero
CWCs play an important role as life-history critical habitats and Marin, this volume), conservation and effective manage-
for fish species. Considering that an Essential Fish Habitat ment of this VME remain challenging due to the difficulties
(EFH) can be defined as “those waters and substrates neces- in controlling the fishing activities in the international
sary to fish for spawning, breeding, feeding, or growth to Mediterranean waters (beyond 12 nautical miles of the
maturity” (Rosenberg et al. 2000), there is enough evidence coast). In the SML CWC province, a refuge effect from fish-
of the role of CWCs as EFHs. ing has been shown for some commercial species distributed
in the coral areas (D’Onghia et al. 2010, 2012), but trawlers
still often fish inside the FRA with the aim of obtaining
30.5.2 Fishing Impact greater catches and larger sizes of commercial species
(D’Onghia et al. 2017).
The CWC habitats are valuable fishing areas as large sizes Due to the slow recovery rates of CWCs, the habitats that
and high abundances of commercial fish species often occur they build are highly vulnerable and may take many decades
in these habitats. Thus, CWC habitats are often impacted by or centuries to recover from damage (e.g. Roberts 2002;
commercial fishing (e.g. Roberts et al. 2000; Fosså et al. Freiwald et al. 2004; Shester and Ayers 2005). Considering
2002; Hall-Spencer et al. 2002; Reed 2002; Roberts 2002; that fishing activity is carried out using different fishing tech-
Grehan et al. 2005; Wheeler et al. 2005b; Buhl-Mortensen niques and targeting different species both on muddy and
et al. 2010; Bo et al. 2014a; D’Onghia et al. 2017; Hinz 2017; rocky bottoms, knowledge of CWC habitat location and their
Otero and Marin this volume). The fishing activity in CWC relative use by fish species is of utmost importance for the
areas can cause both direct effects of fishing on the stocks and development of effective management and conservation
direct and indirect effects of fishing on the habitat, which can measures. In this regard, in order to increase the knowledge
then further impact stocks (Armstrong and Falk-Petersen and promote an effective ecosystem-based fishery manage-
2008; Armstrong et al. 2009, 2014). Clear examples of coral ment of the deep sea (Rosenberg et al. 2000; Grehan et al.
degradation and consequent reduction in economically 2009, 2017), a large-scale monitoring of the fishing impact
important species have been reported in some studies (e.g. on CWCs needs to be properly implemented as part of
Koenig et al. 2000; Reed et al. 2005; Du Preez and Tunnicliffe Marine Strategy Framework Directive.
2011). In relation to trawling activity carried out on Learmonth
Bank off northern British Columbia and the consequent Acknowledgements The author wishes to thank Francesca Capezzuto
reduction of rockfish, Du Preez and Tunnicliffe (2011) con- for her collaboration in selecting the papers, Daniela Potenza for setting
up the tables/figures and the editors, Covadonga Orejas and Carlos
cluded that the degradation of biogenic structures is a long- Jiménez, for their constructive comments on the manuscript. The author
term detriment to rockfish species and, although the is also grateful to J.H. Fosså, T. Kutti (Institute of Marine Research,
mechanism remains unclear, their observations suggest that it Norway), A. Grehan (National University of Ireland, Galway)
occurs through the destruction of a habitat that is more effec- (CoralFISH Gallery: Marine Research Institute of Iceland; OceanLab –
University of Aberdeen; Royal Netherlands Institute of Sea Research)
tive for shelter than rough inert seafloor. and P. Marin (OCEANA) for photo courtesy.
Foley et al. (2010) used a production function approach to
capture the functional values provided by CWC communi-
ties, such as habitat, spawning grounds, nursery and refuge
to commercial species of redfish (Sebastes spp.). They found References
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Joana Boavida, Ronan Becheler, Anna Maria Addamo,

Florent Sylvestre, and Sophie Arnaud-Haond
Abstract caused by vicariance or local adaptation. However, prog-

Given the vastness of the oceans and the small size of ress has been made that is allowing researchers to retrace
larvae and other marine propagules, tracking marine past major modifications in the patterns of cold-water
organisms’ dispersal particles is unrealistic. When propa- coral migrations at evolutionary time-scales, in and out of
gules successfully recruit, a genetic profile can be tracked the Mediterranean Sea. Growing evidence of the influ-
that integrates the movements of multiple generations. ence of clonality and its effect on estimates of genetic
Molecular analyses thus provide an indirect means of diversity now stimulate researchers to engage in opti-
estimating connectivity among subdivided populations, at mised sampling strategies. Improved estimates are possi-
any given spatial and/or temporal scale of interest. In gen- ble to attain, provided a rigorous sampling strategy.
eral, it remains challenging to disentangle the relative Studies of the cosmopolitan corals Lophelia pertusa and
influence of the various processes that cause the observed Madrepora oculata have made evident that Atlantic popu-
patterns of genetic differentiation among subpopulations, lations are clearly differentiated from Mediterranean
notably in far-off deep-sea environments. In the past ones, suggesting that contemporary gene flow between
decade only a handful of studies have reported on the the two genetic backgrounds is very limited, if at all pres-
genetic patterns in Mediterranean cold-water corals. This ent. Results support several non-mutually exclusive
represents a substantial limitation for any researcher hypotheses: that subpopulations in the North East Atlantic
attempting to understand the dynamics of Mediterranean were recolonised from Mediterranean refugia following
cold-water coral populations. It affects as well conserva- the last glacial maximum; that Mediterranean L. pertusa
tion decisions involving these vulnerable species and reefs appear to have been relevant glacial refugia during
habitats. Until recently, hypotheses for gene flow of some the Pleistocene glaciations and the main source for North
deep-sea corals in the Atlantic have included moderate to East Atlantic recolonisation; and that M. oculata in the
high connectivity at broad and regional scales, through NE Atlantic may have had multiple sources of post-Last
sporadic larval transport mediated by ocean currents, and Glacial Maximum colonisation, which remain elusive.
simultaneous strong discontinuities between ocean basins The solitary Desmophyllum dianthus has been shown to
share the same genetic identity between very distant pop-
ulations (Mediterranean and NE Atlantic). Yet, it remains
J. Boavida · F. Sylvestre · S. Arnaud-Haond (*) unclear if this is solely due to high contemporary gene
Ifremer, UMR MARBEC (Marine Biodiversity, Exploitation and
Conservation), Sète Cedex, France flow or if the genetic resemblance is a remnant left by an
e-mail: [email protected] Atlantic post-glacial recolonisation from a unique
R. Becheler Mediterranean source with high population size. Future
Ifremer, Département Etude des Ecosystèmes Profonds, genome-wide studies with next generation sequencing
Laboratoire Environnement Profond, Centre de Brest PLOUZANE techniques will undoubtedly help clarifying the interpre-
France; Centro de Conservación Marina, Departamento de tations of molecular data in terms of past and present
Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad
Católica de Chile, Santiago, Chile cold-water corals migration pathways. This is strongly
needed, as the development of effective conservation
A. M. Addamo
Department of Biodiversity and Evolutionary Biology, National strategies relies on well-informed, knowledge-based,
Museum of Natural Sciences (MNCN-CSIC), Madrid, Spain policies. These must include thorough species invento-

https://doi.org/10.1007/978-3-319-91608-8_31
358 J. Boavida et al.
ries, relatedness, connectivity metrics and clear identifica- (Freiwald et al. 2009; Orejas et al. 2009; Mytilineou et al.
tion of genetic units, all of which depending on the use of 2014). A diversity of species have been used to reconstruct
robust techniques. Indeed, information on the genetic the past history of the Mediterranean Sea (Montagna et al.
connectivity of Mediterranean cold-water coral popula- 2006; Frank et al. 2011). Nevertheless, mainly three species
tions has proven to be key to the establishment of a pro- (Lophelia pertusa, M. oculata and D. dianthus) could be col-
tected site under the European Union’s Natura 2000 lected with sufficient numbers of specimens to allow the
Network of protected areas. We conclude with perspec- indirect genetic reconstruction of past and present connectiv-
tives on how Next Generation Sequencing will strengthen ity of Mediterranean CWCs and their present and past
inferences on connectivity of the majestic cold-water exchanges with Atlantic coral specimens.
coral habitats in the coming years. One of the particularities of most corals is their ability to
reproduce sexually and asexually. Partial asexuality (“clon-
Keywords ality”) complicates both the dynamics and evolution of pop-
Population genetics · Clonality · Connectivity · Next ulations and the strategies needed to sample and to analyse
generation sequencing molecular data to allow interpretations in a population
genetics framework. It is thus important to explicitly take
asexual reproduction into account in sampling designs, data
analyses and interpretations (Halkett et al. 2005; Arnaud-
31.1 Introduction Haond et al. 2007).
This chapter will first tackle clonality and its implication
Connectivity designates many different aspects of movement for adequate sampling, before engaging into a synthesis of
in ecology. Landscape connectivity is defined as ‘the degree previous work on the population genetics of CWCs (with a
to which the landscape facilitates or impedes movement focus on scleractinians) in the Mediterranean Sea, and their
among resource patches’ (Taylor et al. 1993). More relevant connection to Atlantic populations. The scarce number of
to population genetics, connectivity is designated by studies published thus far on Mediterranean CWCs and a
Moilanen and Hanski (2001) as “typically related to the number of important pitfalls associated with life history
migration rate and gene flow among populations and coloni- traits of corals led us to offer a synthesis of the limited avail-
sation of empty habitat”. Before engaging into this synthesis able data. However, here we give a roadmap for future stud-
it is essential to clarify that the choice of sampling, molecu- ies: We point the reader to optimised sampling schemes and
lar and analytical methods impose important differences in identify new research avenues opened by the new generation
the inferred level of population connectivity (past or present) of molecular data -offered by next generation sequencing
and interdependence (demographic or evolutionary) revealed (NGS)- and computational analyses.
by molecular estimates (Waples and Gaggiotti 2006; Lowe
and Allendorf 2010). In this chapter, the wording “past, pres-
ent and future connectivity” embeds on one hand the evolu- 31.2 Considerations for Sampling
tionary history, present day migration and future modification and Clonality
owing to environmental changes, and on the other the con-
stant improvement of molecular tools used to infer those pat- Partial asexuality (clonality) characterises most coral spe-
terns, and the way this progress can modify our perception cies: they can reproduce sexually through the production of
and inferences. gametes and recombination, or clonally through the produc-
Numerous reports of fossils of several species of cold- tion of colonies sharing the same genome (except for somatic
water corals (CWCs) within and surrounding the mutations) by fragmentation or parthenogenesis. Clonality is
Mediterranean Sea (Malinverno et al. 2010; Perrin and an essential aspect to consider when engaging into a popula-
Bosellini 2012) have guided sampling for use as archives to tion genetics study on corals. It does not only affect the path
retrace past climates. Yet, only scarce remotely operated for gene transmission, the dynamics of populations at differ-
vehicle (ROV) exploration has been performed thus far in ent stages of colonisation or demographic equilibrium, but
canyons and seamounts (e.g. Danovaro et al. 2010; Fabri also their resistance and resilience, and their evolution. More
et al. 2017; Aymà et al., this volume; Lastras et al., this vol- pragmatically for the researcher, it also affects the way sam-
ume), features susceptible of hosting living corals. Living- pling should be planned and molecular data interpreted in a
records, however, spread across the entire Mediterranean. population genetics framework. Actually, the population
These are dominated by Madrepora oculata (Orejas et al. genetics framework was designed and developed for pure
2009; Gori et al. 2013; Lastras et al. 2016; Fabri et al. 2017), sexual organisms and requires dealing with individual geno-
which seems to better resist environmental changes types, thus recognising individuals at the demographic and
(Wienberg et al. 2010), and Desmophyllum dianthus genetic scale (reviewed in Arnaud-Haond et al. 2007).
31 Past, Present and Future Connectivity of Mediterranean Cold-Water Corals 359
31.2.1 Clonality and Sampling Strategy Estimates of clonal versus sexual reproduction as well as
genetic diversity would obviously suffer serious biases, with
In terms of sampling strategy, working on partially asexual some of the individuals being overrepresented due to their
organisms imposes strong constraints on the sampling large size or position in the middle of the gear trajectory.
design (Arnaud-Haond et al. 2007). When researchers are Submersible or ROV based sampling, with well annotated
interested in appraising the imprint of clonality on the videos and/or organised sampling material (like drawers
dynamics of populations, they should go for an explicit, with individual and/or labelled cases; see Becheler et al.
standardised sampling scale (i.e. standardising the sampled 2017; Orejas et al. 2017), allow a good traceability which is
area among reefs), and randomised spatial sampling at an required. Additionally, accidental bycatch with longlines can
accurate spatial scale, in order to be able to compare results provide interesting samples. These may be associated to
obtained in different reefs or coral gardens. The sampling approximate GPS coordinates and thus valuable, once the
scale should be nested based on previous knowledge of the extent of clonality has been appraised during pilot or previ-
size of genets (i.e. the extent of a genetic individual issued ous studies.
from a single zygote that spreads spatially and temporally
through clonality by producing modules, called ramets), or
the dispersal of clonal propagules. When such knowledge is 31.2.2 Clonality and Population Genetics:
not available it is highly recommended to perform pilot Beware of Bush Mosaicism
studies with nested sampling scales in order to appraise the and the Strategy with Genetic
spatial extent of the influence of clonality for the species Replicates
considered. When researchers are not necessarily interested
in appraising the extent of clonality but are just focused on A peculiarity of corals is their ability to form coral bushes
basic genetic analysis to estimate genetic diversity and (also termed “patches” and “thickets”). This capacity was
structure, they may favor a coarse sampling of ramets with a confirmed for CWCs in the North Atlantic (Wilson 1979,
haphazard strategy, and exclude replicates of the same gen- Reed et al. 2007) and, more recently, through the description
otypes (i.e. belonging to the same genet) if still occurring in of mosaic colonies of M. oculata and L. pertusa growing on
the final dataset. Making the a priori choice of ignoring each other (Arnaud-Haond et al. 2017). In the same way,
clonality can be imposed by technical limitations when conspecific colonies of different colors have been observed
sampling, which are particularly acute in deep-sea research. on the field, for which mosaicism was confirmed by genotyp-
It is however not necessarily recommended, as clonality can ing of L. pertusa (Hennige et al. 2014). The occurrence of
have strong implications in the spatial distribution of poly- such coral bushes implies that additional caution is necessary
morphism and in its temporal evolution. At least in such when sampling: to examine the shape of colonies and possi-
cases, the unique geographical coordinates of each colony ble anastomosed branching is fundamental, in order to avoid
should be kept in order to attempt assessing the scale of mixing genets in the lab, which would mix genotypes, mak-
clonal spread/dispersal on the basis of the best possible ing it impossible to reconstruct individuals a posteriori.
sampling in hand. A notable practical example of this strat- Estimating gene flow requires the access to a random and
egy was given for Lophelia pertusa reefs along the Bay of representative sampling of the populations studied, with
Biscay (Becheler et al. 2017). Despite a general low inci- demographic units represented only once. Now, the delinea-
dence of clonality, sampling colonies separated by at least tion of what is a “demographic unit” depends on the path of
150 m showed identical genotypes suggesting a rather long sexual reproduction and on the independent or entangled
dispersal distance. fates of ramets. Once the colonies are discriminated and the
The choice of sampling gear is also essential to allow iso- level of clonality is assessed, one will engage in a population
lating georeferenced colonies sampled on the sea floor, dis- genetics analysis in a different way depending on the path
criminating them on the deck and analysing them individually of asexual reproduction. For most clonal plants including
in the laboratory. Trawls, dredge or even ledges are thus to be seagrasses, where modules –ramets- of the same genetic
avoided for various reasons. Leaving aside the interesting individual –genet- remain connected and potentially meta-
and fundamental debates on the ethic of trawling reefs for bolically interdependent for some time (Salzman and Parker
scientific purposes, fragments of colonies sampled through 1985; Alpert 1996; Arnaud-Haond et al. 2012), the choice of
trawling or dredging cannot be easily teased apart on the keeping or discarding replicates in the dataset before esti-
deck, preventing the appraisal of clonality in the collected mating population genetic structure can be debated. Each of
sample. In other words, sampling a coral reef or a coral gar- these choices implies underlying assumptions: the lack of a
den with such gear can be compared to the sampling of tropi- relationship between the reproductive success and the size
cal forests with a bulldozer, followed by the blind genotyping (in terms of number of ramets) of genets, none of which are
of broken branches. usually tested for the species and populations at stake. For
corals, the question at hand is a little different: distinct colo- for reefs in the western basin of the Mediterranean Sea, as
nies in the same area can be considered as independent meta- well as in the Gulf of Cádiz (GoC) and Moroccan margin
bolic and reproductive units, whether or not they share the (Schroder-Ritzrau et al. 2005), even if a relative decline is
same genotype, and thus be included for connectivity esti- reported since the end of the Last Glacial Maximum (LGM)
mates. It is thus reasonable in most cases, provided sampled (Taviani et al. 2011), 10,000–12,000 years ago. An opposite
colonies were well discriminated in the field (see above), to situation was suspected in Northeast (NE) Atlantic, where
engage into connectivity estimates based on the full dataset. climatic fluctuations were suggested to be the main driver of
geographic distribution and development of reefs. In this
region, Ice Ages hampered the growth of CWC reefs (Frank
31.3 Case Studies et al. 2011).
Studies of demography, population structure, and repro-
31.3.1 Context duction of CWCs are rather scarce (but see Brooke and
Young 2003; Waller 2005; Larsson et al. 2014; Pires et al.
Despite the fast technological progress that has allowed 2014; Bramanti et al., this volume; Lartaud et al., this vol-
improved access to the deep-sea, these ecosystems remain ume; Reynaud and Ferrier-Pagès, this volume), as generally
hard to explore and information about connectivity is still applies with other deep-water organisms. However, it is well
scarce. For example, direct tracking of free living marine known that understanding the connectivity of marine popula-
larvae is highly challenging in coastal species (but see tions is vital for conservation and fisheries management, par-
Thorrold et al. 2007), and virtually impossible for species ticularly for the strategic design of marine reserves
such as CWCs (but see recent progress in Orejas et al., this (Hedgecock et al. 2007) or for the sustainable use of marine
volume). The use of genetic markers is necessary to obtain resources (e.g. implementation of sea-based wind farms and
an indirect mean of levels of connectivity. In this context, their environmental impact on benthic communities, see for
population genetics offers the theoretical framework to indi- example the European project CoCoNET http://www.
rectly assess connectivity through the analysis of the distri- coconet-fp7.eu/).
bution of genetic variation (“polymorphism”), in order to
infer the degree of inter-dependence of discretely distrib-
uted CWC reefs. 31.3.2 Madrepora oculata and Lophelia
Contemporary genetic processes, such as migration and pertusa: Out and
population size, contribute to explaining the present-day Into the Mediterranean
distribution of neutral genetic diversity (i.e. not subject to
selection) within species ranges. Yet, past events, such as The two reef-building CWCs, L. pertusa and M. oculata, are
fluctuations of geographic ranges, demographic bottle- suspected to have recolonised the NE-Atlantic from the
necks and/or expansions, can leave strong and persistent Mediterranean at the end of the last glacial episode (De Mol
genetic signatures, still detectable today and thus imping- et al. 2005; Henry et al. 2014), after a long period of scarcity
ing the present day study of the distribution of genetic or extirpation during the late Pleistocene (see Taviani et al.,
polymorphism (Hewitt 2000, 2004). Understanding a pat- this volume; Vertino et al., this volume; other chapters from
tern of genetic structure and appraising the present day the past section in this same volume).
level of genetic connectivity among populations, thus In the work we summarise here, we aimed at addressing
requires considering and discriminating both present and those hypotheses about past connectivity by unraveling the
past events affecting the demography of species and the genetic differentiation, or the lack of, of CWC populations in
present day distribution of their genetic diversity as well as the Mediterranean and in the Atlantic Ocean.
the evolutionary forces driving it (Bierne et al. 2011;
Gagnaire et al. 2015). 31.3.2.1 Sampling Locations and Strategy
Geological records and isotopic dating of sediment and As explained above, clonal organisms require an adequate
coral remains have delivered most of the knowledge about sampling strategy, which is particularly hard to apply in the
the paleogeography of CWC. The Mediterranean Basin is an deep-sea. This is probably one of the main barriers to gather-
historical area for CWC presence (Freiwald et al. 2004; Di ing robust information about the clonal architecture and pop-
Geronimo et al. 2005; Taviani et al. 2005; Montagna and ulation genetics of CWC populations. In 2011, during the
Taviani, this volume; Rebesco and Taviani, this volume; cruise BobEco (European Project CoralFish, Research Vessel
Taviani et al., this volume; Vertino et al., this volume) where RV Pourquoi-Pas?), the scientific team experimented a chal-
the occurrence of deep reefs has been recognised to be con- lenging sampling strategy, allowing a standardised and ran-
tinuous for over 480,000 years (McCulloch et al. 2010). The domised collection of 25–30 colonies per site of both L.
last 50,000 years may correspond to an active growth period pertusa and M. oculata (Becheler et al. 2017). Five canyons
from the Bay of Biscay (European continental margin) and regional, pattern of genetic structure was observed among M.
one location within the Logachev Mounds (Rockall bank) oculata reefs, with several differentiated units detected in the
were sampled in this way. In 2012, the same strategy was Atlantic.
used in two locations in South Iceland (European project The ability to disperse may be lower for M. oculata than
Hermione, RV Thalassa). The sampling strategy consisted of for L. pertusa. In this case, the gene flow among regions
a sampling quadrat of 200 * 100 m2. Then, 30 X-Y coordi- would be too low to homogenise the genetically diverging
nates were randomly generated within each quadrat (with units. Unfortunately, despite its apparently rather widespread
0 < X < 200 m and 0 < Y < 100 m). They corresponded to the distribution (Arnaud-Haond et al. 2017), M. oculata has thus
geographical coordinates of each sampling unit. Such stan- far retained less attention than L. pertusa and knowledge is
dard strategy, based on known and random spatial coordi- lacking about its larval biology. Another, non-mutually
nates, allowed acquiring high-resolution quantitative exclusive hypothesis can also be formulated: the influence of
information about the association among coral species, nota- past events, such as the Last Glacial Maximum, which may
bly its spatial extent (Arnaud-Haond et al. 2007), for three have differently affected these two species, depending on
regions of the NE-Atlantic. All theoretical and practical their physiological tolerance (see Reynaud and Ferrier-
details about this strategy can be found in Becheler et al. Pagès, this volume) and consequent location of the refuges
(2017). that would be at the origin of present day Atlantic
Yet, such sampling is technically complex and time con- populations.
suming, requiring cruises partly devoted to genetic purposes.
Most samples, notably those from the Mediterranean inte- 31.3.2.3 Past Glacial Events and Their Influence
grated in this study (Santa Maria di Leuca -Ionian Sea, and on Shared and Unique Polymorphism
Canyon of Lacaze-Duthiers –Gulf of Lions, northwestern Between the Mediterranean
Mediterranean) were indeed collected in an “opportunistic” and the Atlantic
way, either during exploratory transects, or within sediment The ITS sequences delivered complementary information to
collected with cores or grabs. We could thus retrace popula- that obtained based on microsatellites. Their rate of evolu-
tion genetics and connectivity of Mediterranean and Atlantic tion being lower than for microsatellites (Hillis and Dixon
reefs, but could not compare the clonal architecture in the 1991; Balloux and Lugon-Moulin 2002), they may be infor-
Mediterranean and the Atlantic due to the limitation imposed mative for larger temporal and spatial scales. For L. pertusa,
by the opportunistic sampling strategy. the haplotype network (Fig. 31.1) revealed two main haplo-
types, essentially found in the Mediterranean, Bay of Biscay
31.3.2.2 Present-Day Genetic Differentiation and in Iceland. Closely related haplotypes separated by few
Between Mediterranean and North-East mutations were found in low frequency around the main hap-
Atlantic lotypes and they originated from the Bay of Biscay, Ireland,
The genetic structure of both L. pertusa and M. oculata was and Iceland. This L. pertusa haplotype network is organised
assessed through the use of two types of nuclear markers, i.e. as a typical “star-like cluster” often recognised as a signature
a set of respectively seven and six microsatellites, and inter- of ‘recent’ demographic expansion (Teixeira et al. 2011).
nal transcribed spacer (ITS) sequences (Becheler 2013). For Additionally, the main haplotypes are shared between the
both species, Atlantic populations appeared divergent from putative source(s) of recolonisation and recolonised areas.
Mediterranean ones (Fig. 31.1). For example for L. pertusa Satellite haplotypes are generated within populations having
the fixation index (FST, estimated with microsatellites) demographically expanded, which together with the signifi-
between a Mediterranean and an Atlantic population is cant results obtained using the Fu and Li tests (Fu and Li
around ten times higher than a FST between two Atlantic pop- 1993), support the hypothesis of a recent demographic
ulations, and two to three times higher for M. oculata. expansion in NE Atlantic populations.
Yet, in the open NE-Atlantic, patterns of genetic structure The network built with M. oculata’s ITS haplotypes
are strikingly different between these two species. Atlantic shows a very different pattern, with a chaotic distribution of
populations of L. pertusa appeared as a large and single pan- frequent and rare haplotypes, and private (endemic) haplo-
mictic unit, i.e. one where all individuals are randomly mat- types found in all regions. The more frequent haplotypes are
ing, with no clear genetic differences among reefs of the Bay numerous and can alternatively appear as shared between
of Biscay, Logachev Mounds and Iceland. In this context, it two, three, four or five regions. Notably, several Mediterranean
is worthy to mention that experiments in aquaria have haplotypes are shared by specimens collected in the Azores
recently reported that larval duration can reach 5 weeks and (central NE Atlantic), the Bay of Biscay, Ireland and in South
that larvae were active swimmers (Larsson et al. 2014). Iceland, suggesting a possible common history and/or an
Results observed here support the hypothesis that high dis- ancient genetic connection, whereas they are not shared with
persal potential is realised in the wild. Contrastingly, a the Mediterranean.
Lophelia pertusa Madrepora oculata
Icl Icl
Irl
Irl Icl
Irl
BoB
Med
Az MOW BoB
BoB
Mediterranean
Azores
Bay of Biscay
Ireland
Iceland
Az
Med
Med
Fig. 31.1 Summarised insight of the known phylogeography of two were based on multi-locus microsatellite genotypes. Below, the internal
relevant reef forming cold-water corals (CWCs), Lophelia pertusa (on transcribed spacer (ITS) haplotype-networks are provided. Each circle
the left) and Madrepora oculata (on the right). Black points are located corresponds to one haplotype, while its size is proportional to the fre-
on sampling sites included in this chapter. Bar plots on the left and the quency of this haplotype within the full dataset. These circles are
right correspond to the clustering analyses (performed with the free divided in colored portions corresponding to the different biogeo-
software TESS). Each multi-colored unitary bar corresponds to the graphic regions. Icl Iceland, Irl Ireland, BoB Bay of Biscay, Az Azores
probability that a genotype belonged to the corresponding cluster, fol- Islands, Med Mediterranean Sea
lowing the idea that one color is for one given cluster. These analyses
If signs of demographic expansions were also detected lotypes observed only in the Atlantic). The homogeneous
within M. oculata’s dataset, this would support a recent pop- genetic background found in the NE-Atlantic with microsat-
ulation expansion/recolonisation in some reefs. The contrast- ellites was also found, although in rare instances, in the
ing present-day genetic structure between L. pertusa and M. Mediterranean (see bar plots on Fig. 31.1 left). This also sug-
oculata and the polymorphism differentially shared among gests a Mediterranean source of recolonisation for the
regions pleads for two different biogeographic scenarios: a NE-Atlantic. The possibly large dispersal ability of L. pertusa
clear support of a Mediterranean origin only for the first spe- larvae may have maintained genetic homogeneity in the
cies, and a pattern calling for a more complex history for the recolonised area of the NE-Atlantic reefs analysed in this
other. study during the last millennia (Boavida et al., under
revision).
31.3.2.4 Biogeographic Scenarios: Two Reef- Madrepora oculata clearly exhibits a more complex pat-
Building Species, Two Distinct Stories? tern likely resulting from marked different historical and
The genetic data obtained for L. pertusa thus supported the present day connectivity. The decline of its populations dur-
hypothesis of De Mol et al. (2005) of a post-glacial (i.e. ing the LGM is very plausible. Nonetheless, the coexistence
<20,000 years ago) recolonisation of Atlantic reefs from a of several genetic backgrounds –and the high number of
Mediterranean refuge. In line with the star-like network main haplotypes- suggests an alternative scenario of post-
observed with ITS haplotypes (Fig. 31.1 bottom left), data LGM recolonisation: despite the fact that the Mediterranean
suggests a (re) colonisation by the main Mediterranean haplo- has likely been a glacial refuge for this species, additional
type, followed by the accumulation of rare mutations during sources of recolonisation in the Atlantic, which remain to be
the post-glacial expansion of Atlantic reefs (the satellite hap- unraveled, may explain this pattern.
31.3.3 Large Scale Connectivity 31.3.3.2 Past and Present-Day Genetic

in Desmophyllum dianthus Polymorphism Between the
Mediterranean and Northeastern
Despite the Mediterranean-wide distribution of D. dianthus, Atlantic Ocean
from the Alborán Sea in the west to the Marmara Sea in the Nuclear and mitochondrial genes have been used as molecu-
east, its low frequency of occurrence (but see recent data in lar markers to determine genetic differentiation, phylogeo-
Fourt et al., this volume; Aymá et al., this volume) limits and graphic patterns and gene flow within and among populations
challenges its study. Nevertheless, several studies have been of D. dianthus in the Mediterranean Sea and the northeastern
conducted in biology, physiology and ecology revealing that Atlantic Ocean. Nevertheless, the internal transcribed spacer
D. dianthus is an exceptional proxy for pH and temperature (ITS), the mitochondrial ribosomal small subunit (16S) and
of water masses in marine ecosystems; It has moderate the cytochrome c oxidase subunit I (COI) were not informa-
tolerance to elevated seawater temperature and to ocean
tive in terms of distinguishing between geographically and
acidification, but there is a clear synergistic impact when bathymetrically isolated populations from global to regional
elevated temperature and pCO2 are combined, resulting in spatial scales (see Fig. 3 in Addamo et al. 2012; Fig. 31.2).
severe reduction of coral metabolism (e.g. Freiwald and The occurrence of shared haplotypes between specimens
Roberts 2005 and references therein; Naumann et al. 2013; could indicate historical patterns of shared genetic diversity
Gori et al. 2016). (current or recent gene flow, incomplete lineage sorting or
The presence of the solitary gregarious coral D. dianthus retention of ancestral polymorphism), methodological bias
(Vertino et al. 2014), or D. cristagalli (synonym, Milne (using genes or regions with a substitution rate inadequate to
Edwards and Haime 1848), has been documented in the show divergence) or both (differences in the coalescence of
Mediterranean since the Early- Middle Miocene. It dwells on these genes combined with population’s divergence; Addamo
hard substrates occurring from the continental shelf to the et al. 2012). To assess the population genetic structure and
upper bathyal zone, commonly associated to scleractinian the ability of this species to disperse into different regions
reef framework-forming CWCs in what was described as a and habitats, contributing to the local gene pool (i.e. migra-
“white coral” triad of Lophelia-Madrepora-Desmophyllum tion), nuclear microsatellite sequences have provided ade-
(Pérès and Picard 1964; Zibrowius 1980; Roberts et al. 2009; quate resolution. Markers with higher evolutionary rates –
Chimienti et al., this volume). Macrohabitats of the coral such as microsatellites – have been developed for D. dian-
framework consist of continuous aggregations of branched thus (Addamo et al. 2015). They allowed the assessment of
scleractinian coral colonies (primarily M. oculata and sec- connectivity among populations dwelling at different depths
ondarily L. pertusa), whose skeletons are in mutual contact and to infer biological (e.g. reproduction strategy or larval
with the exception of some small sediment pockets (Savini dispersal) and oceanographic (e.g. bathymetry or water cir-
et al. 2014). The solitary D. dianthus is thought to have been culation) factors driving isolation. No statistically significant
influenced by the Mediterranean Sea’s geologic history in a levels of genetic differentiation have been found among geo-
similar way as the reef-building corals mentioned here graphic populations from the Mediterranean Sea and NE
above, and their co-occurrence is documented in several Atlantic Ocean (Fig. 31.3), suggesting high connectivity
places in the Mediterranean and the Atlantic. Hence, we also among deep-sea locations, with some exceptions for north-
addressed the hypotheses about past (and present) connectiv- ern individuals from the Cantabrian Sea and Ireland.
ity of D. dianthus populations in the Mediterranean and NE
Atlantic through the analysis of genetic polymorphism. 31.3.3.3 Biogeographic Scenarios for D. dianthus
Populations in the Mediterranean Sea
31.3.3.1 Sampling Locations and Strategy and the Atlantic Ocean
Although solitary corals are not colony forming and do not An interpretation of the shared genetic polymorphism
require a complex sampling strategy compared to their colo- between these two marine regions is the hypothesis of a his-
nial counterparts, particular attention is needed in case of torical recolonisation homogenising the gene pools in both
“aggregations” of individuals, where the presence of asexual marine areas. During the Holocene, a colonisation could
(clonal) individual is likely and may interfere with the inter- have taken place from the Mediterranean Sea to the Atlantic
pretation of molecular results. Since all the Mediterranean Ocean with a sufficiently large number of individuals not to
samples of D. dianthus in this study were collected in an have resulted in a genetic differentiation through a founder
“opportunistic” way, as explained above, it is essential to effect (i.e. the dramatic change –and loss- of genetic varia-
apply adequate labels to each ‘ramet’. Samples have been tion that occurs when a population is established in a new
numbered consecutively, except for those forming an “aggre- area by a very small number of migrants not genetically rep-
gation”, where the same number was applied, followed by a resentative of the larger original population).
letter further included in the label in order to identify poten- On the other hand, a physical connectivity along thou-
tial clones during the genetic analyses. sands of miles between the Mediterranean and NE-Atlantic
Fig. 31.2 (a) Study areas:

Mediterranean Sea
a
(orange = Adriatic Sea;
red = Ionian Sea; yellow=strait
of Sicily) and NE-Atlantic
Ocean (light blue=Galicia,
Cantabria and Ireland).
Squares indicate the sampling
locations. (b) Haplotype
network of internal
transcribed spacer (ITS)
ribosomal DNA sequence
haplotypes of Desmophyllum
dianthus belonging to
Mediterranean Sea
populations (orange ) and
NE-Atlantic Ocean
populations (light blue). Sizes
of the circles are proportional
to the number of samples
presenting the same
haplotype. (Adapted from
Addamo et al. 2012) 500 km
Cantabria
PCoA 2 (19.73%)
Mediterranean
Galicia
Ireland
PCoA 1 (52.58%)
Fig. 31.3 Principal coordinate analysis (PcoA) projecting the relative genetic distances among Desmophyllum dianthus populations from the
Mediterranean Sea (red stars) and the Atlantic Ocean (blue hexagons)
Ocean sites may be attributed to the principal currents in rents mainly characterising the Mediterranean Sea and the
intermediate and deep waters (see Fig. 19.18 in Chimienti NE-Atlantic Ocean are the Levantine Intermediate Water
et al., this volume). The intermediate and deep water cur- (LIW), Adriatic Deep Water (AdDW), Aegean Deep Water
currents (AeDW), and Atlantic Water (AW) (Millot and 31.4 A

Complex Biogeographic History
Taupier-Letage 2005). The LIW circulates at approximately Prevents Teasing Apart Remnants
200–600 m along the northeastern slope of the Ionian Sea, of Past Connectivity from Present Day
penetrating into the southern Adriatic Sea, and then contin- Migration
ues along the slope to the Strait of Sicily, where most of it
outflows into the western Basin (at 400 m depth). The other The reason for the results observed here (high homogeneity
two currents (AdDW, AeDW) first accumulate in the troughs of Desmophyllum dianthus between the Atlantic and the
(1000–1500 m) over which they are formed (in the southern Mediterranean compared to a strikingly strong differentia-
Adriatic and southern Aegean Seas, respectively) before tion for Lophelia pertusa and Madrepora oculata) remains
outflowing into the western Basin through various open- to be elucidated. Subject to similar distributions and cur-
ings. These water masses are depth-stratified and may rep- rents, these species may respond differently due to specific
resent two distinct bathymetric levels that could create life history traits. Although largely unknown, these may
depth structuring in species diversity and community com- include a different pelagic larval duration for D. dianthus
position. Nevertheless, the intermediate and deep water and M. oculata relatively to L. pertusa, and/or the solitary
masses circulate and can be identified at greater or lesser versus reef forming nature of these three taxa. Yet, it is also
distances from their zone of origin. They continuously mix likely that differences in their past biogeographical history
and, finally, outflow at the Strait of Gibraltar as a rather have led to the present genetic structure patterns. In order to
homogeneous water (the so called Mediterranean Outflow tease apart the evolutionary scenarios explaining individual
Water, MOW), which is saltier and denser than Atlantic species patterns, and the cause of their strikingly different
water (AW) in that location (Millot et al. 2006). Therefore, levels of differentiation at the scale of European waters,
the Mediterranean Sea is a “machine” that transforms AW molecular data are needed that would deliver a higher statis-
present at the surface just west of the Strait of Gibraltar into tical power to feed data analyses and modelling methods.
denser water that is recognised at 1000–1200 m in most of CWCs in the Mediterranean Sea have a long-term history
the northern Atlantic Ocean (Millot and Taupier-Letage for which the origin is still mostly unknown (but see chapters
2005). The MOW is a saline water mass occupying the of the Past section in this volume). Most Mediterranean
intermediate depths of the NE-Atlantic. It reaches a neu- deep-water fauna was likely extinct during the Miocene due
trally buoyant depth between 800 and 1300 m (Price et al. to the Messinian Salinity Crisis (5.9 Myr ago, Garcia-
1993) and spreads into the North Atlantic: westward to the Castellanos and Villasenor 2011; Freiwald, this volume)
central Atlantic and northward following the coasts of after which the re-opening of the Gibraltar Strait is thought
Portugal and Spain (Bozec et al. 2011; and references to have led to a recolonisation with Atlantic fauna (Bouchet
therein). and Taviani 1992; Hsü et al. 1977). The long-term persis-
Deep-sea and offshore marine protected areas (MPAs) tence of some coral species in the Mediterranean Sea is how-
have been recently recognised by international and ever indicated by fossil data (Fink et al. 2012, 2015; Perrin
national organisations as efficient tools for protection of and Bosellini 2012). Most explorations of CWCs in the
deep habitats (Cordes et al. 2016; Davies et al. 2017; Mediterranean Sea have occurred during the past 15 years.
OSPAR https://www.ospar.org/news/ospar-ministers-pro- The results from these studies reflect a dominance of fossil-
tect-the-north-east-atlantic-deep-seas-treasures; Colombia derived data. Important events of colonisation are likely to
Deep-water Coral National Natural Park designated in have started in the late Pleistocene (Malinverno et al. 2010;
May 2013 by the Ministry of Environment http://www. Taviani et al., this volume; Vertino et al., this volume). At the
parquesnacionales.gov.co/portal/es/parques-nacionales/ end of the Last Glacial Maximum (LGM) coral abundance
parque-nacional-natural-corales-de-profundidad). appears to have declined in the Mediterranean Sea and adja-
Specifically, results from studies on genetic connectivity cent Gulf of Cadiz (Taviani et al. 2011), but episodes of local
of D. dianthus populations in the Mediterranean Sea con- proliferation and contraction varied across basins and spe-
tributed to the classification of a Natura 2000 Site of cies (Fink et al. 2015). In the case of M. oculata, notable
Community Interest (SCI), the centerpiece of the European coral proliferation occurred in the Mediterranean Sea during
Union’s conservation policy, in the southern Tyrrhenian a cold event after the onset of the deglaciation (a period
Sea. This SCI will be used to characterise and define the known as the Younger Dryas 12.9–11.7 kyr ago; Fink et al.
novel concept of cells of ecosystem functioning (Boero 2015). This trend is opposite to the one reconstructed for L.
2015) as conservation and management units, a key con- pertusa in the North East Atlantic (Frank et al. 2011). There,
cept for the definition of networks of MPAs and for the corals disappeared from higher latitudes (approx. >50°N)
identification of suitable areas for off-shore wind farms during periods of major cooling (e.g. LGM), their presence
(Costantini et al. 2017; see also www.coconet-fp7.eu, being largely coincident with warmer conditions. The reap-
CoCoNet EU project). pearance of L. pertusa in higher latitudes is suspected to
have originated from a hypothesised refuge located in the Jarne and Lagoda 1996; Putman and Carbone 2014).
Mediterranean (De Mol et al. 2005; Henry et al. 2014) and/ Microsatellites have proven extremely useful when the ques-
or GoC, including the Moroccan margin (Wienberg et al. tions at hand require a very large number of individuals to be
2010). Surprisingly, as summarised here above, results on M. analysed, but their power strongly depends on the strength of
oculata data point toward other putative refugia, such as the genetic signal and of the density and resolution of the set of
mid-Atlantic seamounts, whereas D. dianthus only gives markers used (Selkoe and Toonen 2006). They do not allow the
signs of present day or recent exchanges across major basins. same level of automatism, cross platform compatibility, and
The phylogenetic reconstruction of the long-term past his- reliability as genome scans when the hypothesis or scenario to
tory of connectivity and recolonisation between the Atlantic be tested requires a high density of markers. The advent of
and the Mediterranean is thus likely to be blurred by multiple NGS offers a novel opportunity to gather genome-scale
events with opposite direction. However, Bayesian recon- sequence information, which may allow a more powerful esti-
structions of high-density genome scans1 using NGS may mate of genetic variation within and among populations and a
help reconstruct complex past scenarios. much higher resolution in the reconstruction of past and pres-
Numerous cases of connectivity estimates have been ent scenarios susceptible to explain the present day distribution
blurred by errors in taxonomic identification or description, of genetic polymorphism. The NGS includes several tech-
including artificial exclusion of species described as differ- niques, most of which have in common the random sequencing
ent on the basis of non-discriminant taxonomic characters, or of DNA, RNA or cDNA (Heather and Chain 2016). Hundreds
in contrast, the inclusion of distinct taxa (Pante et al. 2015a; to thousands of polymorphic genetic markers, behaving as
Altuna and Poliseno, this volume) or even by including semi independent loci, can be retrieved across the entire genome, in
species having developed a certain level of reproductive a relatively simple and affordable manner (price per sequenced
incompatibility (Bierne et al. 2011; Gagnaire et al. 2015). It Gigabase in Goodwin et al. 2016) even for species without a
is now clear that markers used in population genetic studies reference genome. Collectively, these techniques are called
should allow ascertaining the taxonomic status of the taxa at reduced- representation (RR) methods (e.g. Andrews et al.
stake. Teasing apart the signatures of past events such as the 2016) because they target a random subset of the genome (or
last glacial cycles from the ones of present day connectivity transcriptome), rather than sequencing the entire genome
is not a trivial task, especially when relying on a handful of (termed “whole-genome sequencing”), a more costly approach.
markers, as were the cases presented above. Even with the typical small sample sizes as those often limiting
deep-sea studies, by using thousands of independent markers
across the genome, the recent (<10 years) application of NGS
31.5 P
erspectives Arising From Access approaches to deep-water organisms has improved the power
to Genome Scan Data of estimates of demographic parameters in deep-sea octocorals
and population histories (Everett et al. 2016). They also
Traditional phylogenetic and population genetic studies have allowed detection of genomic areas that are under selection in
relied on few molecular sequence markers. These include deep-sea scallops (Van Wyngaarden et al. 2017), and have
mitochondrial and nuclear genes, which can be amplified at resolved deep-sea species radiations and phylogenies (Reitzel
low cost with nearly universal primers. However, they present et al. 2013; Pante et al. 2015a; Herrera and Shank 2016).
some limitations, such as poor genome representation One of the challenges of population genetic -and now
(Angeloni et al. 2012). The use of mitochondrial sequence genomic studies applied to the deep-sea remains the diffi-
markers is further limited in corals due to the remarkable low culty in obtaining a representative number of samples to
rate of mitochondrial genome evolution (Hellberg 2006; make inferences about the evolutionary history of metapopu-
Huang et al. 2008; Shearer and Coffroth 2008). The introduc- lations. Whereas NGS may require fewer samples than clas-
tion of microsatellites in population genetic studies promised sical genetic analyses to obtain robust statistical inferences,
great power to assess similarity between individuals and a similar amount of sampling units and a rigorous sampling
closely related taxa in a cost-effective way, mainly due to their design will remain a requirement with NGS in order to deal
high polymorphism and high mutation rate (Hodel et al. 2016; with clonal diversity, and the consequent best sampling strat-
egy to obtain a representative sample of a population.
Genome scan is used here in its primary semantic meaning, thus fitting
1 Also, while RR techniques provide greater depth of cover-
the definition given by Richard and Hawley (2010, “Human genome”; age (i.e. number of sequences or “reads”), when working on
p 561): “A survey of genetic markers spread across the whole genome. non-model organisms with small genomes (i.e. <0.5 Giga
A genome scan will usually involve hundreds of markers”, rather than
the one previously proposed in the Encyclopedic Reference of base pairs), such as those characterising many CWC species,
Genomics and Proteomics in Molecular Medicine (2006), that narrows assembling draft whole-genomes for reference may become
its scope to the screening for phenotype related markers (“Genome scan another valuable approach. Low-coverage, cost-effective
refers to a genetic research method in which the entire DNA of an methods to produce draft de novo assemblies are already
organism is searched systematically for locations on the chromosomes
that are inherited in the same pattern as a specific trait”). available (Malmstrom et al. 2017), opening a wider range of
possible studies encompassing selection and adaptation The scenarios that could be put forward to explain the pres-
(Ekblom and Wolf 2014), as well as the influence of second- ent-day geographic distribution of polymorphism among pop-
ary contacts (Gagnaire et al. 2015). Finally, having a refer- ulations that we reviewed here for these three relevant species
ence genome in combination with a characterised of CWC scleractinians, are still limited by the level of resolu-
transcriptome (RNA-Seq; Wang et al. 2009) will allow anno- tion of markers used attempting to indirectly reconstruct and
tating the genome for particular genes, permitting the distinc- rank complex biogeographical histories. A higher amount of
tion between selected from neutral variation. Such an information (i.e. loci) is necessary to increase the statistical
approach to pinpoint expressed genes may also assist the fine- power and unravel previously ignored patterns of moderate dif-
tuned identification of appropriate conservation units. The ferentiation, if it exists. As summarised above, moderate levels
combination of these novel techniques with statistical of differentiation may exist for Lophelia pertusa in the Atlantic
approaches that test environment-mediated selection and eco- or Desmophyllum dianthus across the studied range. Besides,
logical niche modelling is likely to trigger a wave of seascape denser sampling of the genome is necessary to reliably recon-
genomics studies (notably reviewed in Riginos and Liggins struct and rank evolutionary scenarios using up to date Bayesian
(2013); Riginos et al. (2016)), highly relevant for CWC con- methods, ideally with approximate dating. These methods may
servation and management. Regardless of the particular van- help to explain the present day patterns of differentiation and to
guard method chosen, for the days that lay ahead, NGS improve understanding regarding present day patterns of con-
encompasses a range of enticing techniques that promise to nectivity. For example, the recent work on the coral-associated
set the scene for deciphering the elusive population contours polychaete Eunice norvegica already shows the increased
of clonal lineages, CWC species and associated fauna. power gained through genome scans (Box 31.1). Similarly,
Box 31.1: Taxonomic Uncertainties Reflect Past and mitochondrial markers (Fig. 31.B3), thus excluding the pos-
Present Day Connectivity in the Polychaete Eunice sibility of male-exclusive migration. RADseq loci (sequenced
norvegica Inhabiting Cold-Water Corals (CWC) Along sites along the genome) avoid issues of developing specific
European Margins markers (such as microsatellites) not necessarily transferra-
The recent (approx. 10 years) development of Next ble between two distant genetic backgrounds, and have
Generation Sequencing (NGS) methods now allows the use increased resolution to reliably reflect the variability of pat-
of an array of genetic markers to analyse the connectivity of terns across the genome. The application of this sequencing
populations. Analysis of nearly 4000 single nucleotide poly- technique also bolstered evidence of a common evolutionary
morphisms (SNP) on the CWC- associated polychaete history dating from before the Last Glacial Maximum
Eunice norvegica (Fig. 31.B1) using Restriction Site (LGM) between individuals as distant as the high latitudes on
Associated sequencing (RADseq, a kind of RR) has con- the North East Atlantic and the central Mediterranean Sea.
firmed limited to non-existent gene flow between Atlantic This new exciting data may represent a harbinger of distinct
and central Mediterranean samples (Fig. 31.B2). It com- high latitudes and Mediterranean refugia for CWC habitats
pletes a previous analysis based on maternally inherited and associated species during past climatic fluctuations.
Fig. 31.B1 Polychaete worms Eunice norvegica. (© Ifremer, Olivier Dugornay, Videocor cruise)
(continued)
Box 31.1 (continued)

Fig. 31.B2 Result from
1.0
admixture ancestry analysis
considering two genetic
0.6 0.8
groups
Ancestry
0.0 0.2 0.4
Bay of Biscay Iceland Mediterranean
Individuals
Fig. 31.B3 COI haplotype NE Atlantic Lineage Mediterranean Lineage

networks of 45 haplotypes.
Each node corresponds to a
haplotype, and is divided
according to its count in each
sampled population
Mediterranean Sea
Bay of Biscay
SE Rockall bank
Iceland
Norway museum voucher
ongoing genomic studies on some of the CWC flagship species longer act on from the ones that are relevant to take into
L. pertusa, M. oculata and D. dianthus promise to hasten our account in the definition of sampling strategies, as well as
understanding of highly contrasting pathways for CWC post- to “promote evolutionary potential and evolutionary pro-
glacial colonisation at the European scale as reported here, to cesses to better protect extant biodiversity and biodiversifi-
further disentangle existing putative cryptic CWC species cation” (Olivieri et al. 2016). Despite the historical local
diversity and to clarify species hypothesis (Addamo, this vol- and temporary extinctions in the Mediterranean and
ume). Recent results indeed suggest that L. pertusa may be a NE-Atlantic, linked to variations in productivity and oxy-
junior synonym of the recently reassigned scientific name of gen levels (Fink et al. 2012, 2015), it is remarkable that
Desmophyllum pertusum (Addamo et al. 2016). Here also, CWC have so swiftly responded to drastic environmental
genome scans are expected to deliver more robust information changes (latitudinal shifts in the order of thousands of kilo-
to dig deeper into this intriguing similarity. meters-wide for L. pertusa and M. oculata, as supported in
Discriminating the imprint of past versus present day the works cited and synthesised here). Coral reappearance
mechanisms acting on the current distribution of genetic has tracked these environmental fluctuations in just a few
diversity is a prerequisite to understand present day drivers hundreds of years (Wienberg et al. 2010). Yet, with the
and patterns of connectivity across their geographic range. cumulative and synergistic effects of environmental oscil-
This information is central to development of informed lations, habitat loss, overexploitation and pollution of the
conservation strategies. Teasing apart past and present driv- deep-sea, this ability to promptly track changes and re-
ers is needed to differentiate between the ones we can no establish/re-adjust their geographical and/or bathymetric
distributions may be hampered, leading to an increased risk Arnaud-Haond S, Duarte CM, Diaz-Almela E, et al (2012) Implications
of extreme life span in clonal organisms: millenary clones in mead-
of extinctions (Harnik et al. 2012). Conservation of CWC ows of the threatened seagrass Posidonia oceanica. PLoS One
benefits from well-informed, knowledge-based decisions, 7:e30454. https://doi.org/10.1371/journal.pone.0030454
for example when it comes to decide how to size and dis- Arnaud-Haond S, van den Beld IMJ, Becheler R, et al (2017) Two “pil-
tribute MPAs. Knowledge must include thorough species lars” of cold-water coral reefs along Atlantic European margins:
prevalent association of Madrepora oculata with Lophelia pertusa,
inventories, which allow for an understanding of their relat- from reef to colony scale. Deep-Sea Res Part 2 Top Stud Oceanogr
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Acknowledgements We wish to thank the following projects, which ity in cold water corals revealed through the novel use of a stan-
contributed through data production or thoughts to feed this synthesis dardized protocol adapted to deep sea sampling. Deep-Sea Res
chapter: CoralFISH EU-FP7 project under Grant agreement no.213144, Part 2 Top Stud Oceanogr 145:120–130. https://doi.org/10.1016/j.
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Drop Chapter
Desmophyllum dianthus Genetics 32
and More
Anna Maria Addamo
Abstract Within the azooxanthellate Scleractinia, the family

The scientific understanding on phylogeny, ecology and Caryophyliidae Dana, 1846 is the most diverse family,
evolution of scleractinian corals has been expanded including 51 extant species and 38 fossil species (Roberts
thanks to the numerous applications of molecular mark- 2009, see online appendix, see Altuna and Poliseno, this
ers. Nevertheless, shallow-water tropical corals were the volume). Representatives of this family include the solitary
main subject of these studies so far. Just recently scien- deep-sea coral Desmophyllum dianthus (Esper, 1794).
tists have focused their attention on deep and cold-water Since D. dianthus is one of the few corals widely
corals. In the last decade, the solitary coral Desmophyllum distributed, several individuals from different areas of both
dianthus (Esper, 1794) has been the subject of several northern and southern hemispheres have been analysed with
studies focused on phylogeny, ecology, and physiology. new developed 30 species-specific microsatellites (Addamo
This drop chapter seeks to summarise the novel obtained et al. 2015a). The population structures, detected either in
results, and consequently the arguments arise, in molecu- northern or southern hemispheres, presented a clear isolation
lar ecology, systematics and evolution of the species. Key by distance model of gene flow (IBD). Nevertheless, ocean
roles of this species in the evolutionary studies of sclerac- currents at different depths are also strongly suspected to
tinian corals are also discussed. play a key role on larval dispersal: (I) as a physical barrier:
e.g. D. dianthus populations, either from New Zealand and
Keywords Chile, presented their own genetic characteristics; or (II) as a
Desmophyllum · Lophelia · Molecular markers · connectivity vector: e.g. gene flow has been detected between
Integrative taxonomy · Molecular ecology individuals from Australia and Argentina, despite their large
geographic distance (Addamo et al., submitted).
Furthermore, in spite of it being well known for its high
morphological plasticity (Fig. 32.1), analyses performed-
The application of molecular markers in the natural sciences based on morphological and morphometric characters of
has enriched and broadened the scientific insight of the natu- skeleton and cnidom-have detected no obvious relationship
ral history and evolution of organisms (see Boavida et al., between the extreme variable morphology and either
this volume). ecological or environmental parameters characterised
In this context, the scientific knowledge on phylogeny, simultaneously (Addamo et al. 2015b).
phylogeography and genetic population of scleractinian cor- Phylogenetically speaking, scleractinian corals belong to
als has been based on - and limited to – principle studies car- two main molecularly defined clades (Romano and Palumbi
ried out mainly on shallow water and tropical species (see 1996), ‘Robusta’ and ‘Complexa’. Molecular data have
e.g. Fukami et al. 2008; Huang et al. 2014). A minority of confirmed D. dianthus belongs to the major clade ‘Robusta’
works has involved deep-sea and azooxanthellate corals (e.g. and in one of the polyphyletic clades of family Caryophylliidae
Stolarski et al. 2011 and reference therein) that compose half (Addamo et al. 2012).
of the total number of corals species identified so far. However, an in-depth comparative morphological and
molecular analyses – including skeletal ontogeny,
micromorphological (septal ad wall granulations) and
A. M. Addamo (*) microstructural (arrangement of rapid accretion deposits,
Department of Biodiversity and Evolutionary Biology, National thickening deposits) characters, and several nuclear and
Museum of Natural Sciences (MNCN-CSIC), Madrid, Spain

https://doi.org/10.1007/978-3-319-91608-8_32
374 A. M. Addamo
Fig. 32.1 Morphological
variability of calice and
corallum in Desmophyllum
dianthus. Origin of
specimens: Chile (a–c, e, j);
New Zealand (d, g); Ecuador
(i); Japan (f, k); New
Caledonia (h). (See Addamo
et al. 2015b for further details,
© Elsevier)
mitochondrial m olecular markers, characterised by different colonialism versus solitary way development in corals are
mutation rates and polymorphism level – contributed to cases in point.
clarify the phylogenetic relationship between D. dianthus A variety of studies has been performed using D. dianthus
and its closely related species (Addamo et al. 2016). Indeed, as a model organism to study the synergistic effect of global
this study revealed a surprising genetic similarity between D. change stressors as ocean acidification and sea temperature
dianthus and the largest colonial azooxanthellate species of rise (e.g. Gori et al. 2016; Reynaud and Ferrier-Pagès, this
coral in the deep-sea waters, Lophelia pertusa, which has volume). Moreover, this species has been considered as a
been recently suggested as junior synonym of Desmophyllum palaeoclimate and palaeonvironment archive to trace ele-
pertusum (Linnaeus, 1758) nov. comb. (see Addamo et al. ment (B/Ca, Mg/Ca, Sr/Ca, and U/Ca) (e.g. Montagna et al.
2016 for further details). 2008, Montagna and Taviani, this volume) and as well as to
The genus adscription shift and the consequences of such reconstruct seawater pH over the past thousands year (e.g.
unanticipated synonymy should fosters even more to the Stewart et al. 2016).
scientific community to provide a deep revision of taxo- Despite the difficulties encountered in ecological features
nomic identification key of Scleractinia. For example, argu- (e.g. gathering significant collections from the deep-sea) or
ments for a dual morphology-molecular approach, the laboratory settings (e.g. keep or breed them in aquaria), D
dianthus has been proved being an interesting species for
32 Desmophyllum dianthus Genetics and More 375
genomics as well as ecological and experimental analysis, Cnidaria). PLoS One 3:e3222. https://doi.org/10.1371/journal.
pone.0003222
giving insight into the general principles of a broad range of Gori A, Ferrier-Pagès C, Henninge SJ, et al (2016) Physiological
various disciplines, such as genetics, development and response of the cold-water coral Desmophyllum dianthus to
evolution. thermal stress and ocean acidification. PeerJ 4:e1606. https://doi.
org/10.7717/peerj.1606
Huang D, Benzoni F, Fukami F, et al (2014) Taxonomic classification
Acknowledgments I thank the reviewers Sophie Arnaud-Haond and
of the reef coral families Merulinidae, Montastraeidae, and
Federica Costantini and the editor Covadonga Orejas for their valuable
Diploastraeidae (Cnidaria: Anthozoa: Scleractinia). Zool J Linn
and insightful comments that improved the manuscript. I want to
Soc-Lond 171:277–355. https://doi.org/10.1111/zoj.12140
express my deep gratitude to Agostina Vertino, Jaroslaw Stolarski,
Montagna P, McCulloch M, Mazzoli C, et al (2008) High-resolution
Annie Machodorm and her group members at the Department of
geochemical records from Mediterranean cold-water corals: proxies
Biodiversity and Evolutionary Biology of MNCN, for their great
for paleoclimate and paleoenvironmental reconstructions and the
support and the inspiring discussions. This research was supported by
role of coral physiology. CIESM Work Monogr 36:55–60
the Spanish Ministry of Science and Innovation (CGL2011-23306 and
Roberts JM, Wheeler AJ, Freiwald A, et al (2009) Cold-water corals:
CTM2014-57949R) and EU CoCoNET—“Towards COast to COast
the biology and geology of deep-sea coral habitats. Cambridge
NETworks of marine protected areas (from the shore to the high and
University Press, New York, p 334. https://doi.org/10.1017/
deep-sea), coupled with sea-based wind energy potential”—from the
CBO9780511581588
VII FP of the European Commission under grant agreement n° 287844.
Romano SL, Palumbi RS (1996) Evolution of Scleractinian corals
inferred from molecular systematics. Science 271:640–642. https://
doi.org/10.1126/science.271.5249.640
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Desmophyllum and colonial Lophelia. BMC Evol Biol 16. https:// patterns, drivers and fate in a technically and environmentally
doi.org/10.1186/s12862-016-0654-8 changing world
Addamo AM, Miller K, Haüssermann V et al Global-scale genetic Montagna P, Taviani M (this volume) Mediterranean cold-water corals
structure of cosmopolitan cold-water coral species (under review) as paleoclimate archives
Fukami H, Chen CA, Budd AF, et al (2008) Mitochondrial and nuclear Reynaud S, Ferrier-Pagès C (this volume) Biology and ecophysiology
genes suggest that stony corals are monophyletic but most families of Mediterranean cold-water corals
of stony corals are not (Order Scleractinia, Class Anthozoa, Phylum
Diversity of Bacteria Associated
with the Cold Water Corals Lophelia 33
pertusa and Madrepora oculata
Markus G. Weinbauer, Davide Oregioni, Anne Großkurth,

Marie-Emanuelle Kerros, Tilmann Harder,
Michael DuBow, Jean-Pierre Gattuso, and Cornelia Maier
Abstract the Mediterranean Sea and the North Atlantic for both
Recent research suggests that corals including cold- coral species, however, this depends on the phyloge-
water corals harbor a diverse community of bacteria netic levels applied. In addition, there was also indica-
that are not only pathogens but also potential mutual- tion for a shared microbiome between the Mediterranean
ists. Here we review data on bacterial community com- Sea and the Atlantic. Therefore species-specific bacte-
position and diversity on the main cold-water corals rial associations seem to exist, whereas the biogeo-
framework builder species: Lophelia pertusa and graphical variability can be seen as adaptation to
Madrepora oculata. Sampling strategies such as box specific environmental conditions.
core, video grabs and remotely operated vehicle did not
reveal strong differences between bacterial community Keywords
composition as long as samples were used that looked Fingerprints · Pyrosequencing · Biogeography ·
‘not contaminated’. However, there were strong differ- Microenvironments · Core microbiome
ences of bacterial diversity between the two coral spe-
cies. An analysis of bacterial community composition
by pyrosequencing of L. pertusa and M. oculata
revealed for the Mediterranean Sea the presence of the 33.1 Introduction
potential mutualists already found in the Atlantic indi-
cating a species-specific core microbiome. The data Tropical corals have been intensively investigated e.g. with
also suggest some biogeographical differences between respect to their associations with algae, their ecology and the
ecosystem they populate. However, it is not until compara-
tively recent (around two decades ago) that the attention has
M. G. Weinbauer (*) · D. Oregioni · M.-E. Kerros · C. Maier also focused on corals inhabiting the dark cold-water ecosys-
Sorbonne Universités, CNRS, Laboratoire d’Océanographie de
tems (e.g. Roberts et al. 2006, 2009). Lophelia pertusa Milne
Villefranche, Villefranche-sur-Mer, France
e-mail: [email protected] Edwards and Haime 1849 (family Caryophylliidae) and
Madrepora oculata Linnaeus 1758 (family Oculinidae) are
A. Großkurth · T. Harder
Bremen Marine Ecology Centre for Research and Education, important species as main frame-builders of such ecosys-
University of Bremen and Section Ecological Chemistry, Alfred tems, which sustain a large biodiversity and biomass of asso-
Wegener Institute for Polar and Marine Research, ciated fauna (e.g. Rogers 1999; Henry and Roberts 2007,
Bremen, Germany
2017; D’Onghia, this volume; Rueda et al., this volume). A
M. DuBow potential threat to cold-water corals (CWCs) is the decrease
Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS
in pH due to increased atmospheric pCO2, since a drop in pH
UMR 9198, Université Paris-Saclay, Université Paris-Sud,
Orsay, France might impair calcification (Maier et al., this volume; Movilla,
this volume; Otero and Marin, this volume). Deep water
J.-P. Gattuso
Sorbonne Universités, CNRS, Laboratoire d’Océanographie de coral ecosystems are abundant above the aragonite saturation
Villefranche, Villefranche-sur-Mer, France level, i.e. the depth where aragonite dissolves (Turley et al.
Institute for Sustainable Development and International Relations, 2007). As predictions indicate that the saturation level will
Sciences Po, Paris, France become shallower due to ocean acidification (OA) (Orr et al.

https://doi.org/10.1007/978-3-319-91608-8_33
378 M. G. Weinbauer et al.
2005; see for a review Maier et al., this volume), the CWC and/or species-specific community of intermediate size and
ecosystems could be negatively affected within the next (iii) a highly variable and huge community reflecting biotic
decades. Also, there are other threats to CWCs such as by and abiotic fluctuations (Hernandez-Agreda et al. 2016, 2017).
pollution, fisheries, oil and gas prospecting and global warm- This has also been suggested for CWCs (Kellogg et al. 2017).
ing (Roberts et al. 2006; Otero and Marin, this volume). Bacteria have been investigated in L. pertusa ecosystems
Lophelia pertusa is a cosmopolitan scleractinian coral (Jensen et al. 2008a, b) and studies on the diversity of bacterial
with a depth range of ca. 50 to >1500 m. Its geographical and associated with are now available (Neulinger et al. 2008, 2009;
depth distribution overlaps with that of M. oculata, although Kellogg et al. 2009, 2017; Schöttner et al. 2009, 2012; van
there are also L. pertusa reefs such as in the Mingulay Reef Bleijsweijk et al. 2015; Meistertzheim et al. 2016). Bacterial
without M. oculata colonies and vice versa (e.g. Rogers 1999; community composition (BCC) has been assessed for M. ocu-
Arnaud-Haond et al. 2015). Madrepora oculata has a weaker lata suggesting that Spongiobacter (now Endozoicomonas)
and more fragile skeleton compared to L. pertusa and is gen- (Neave et al. 2017) could be mutualistic bacteria (Yakimov
erally smaller. Isotope analysis suggests that zooplankton and et al. 2005; Hansson et al. 2009; Meistertzheim et al. 2016).
phytodetritus are the main food sources of these coral species Studies on bacterial diversity on CWCs are also available for
(e.g. Duineveld et al. 2004; Kiriakoulakis et al. 2005; Carlier the Mediterranean Sea (Meistertzheim et al. 2016). Data from
et al. 2009; Roberts et al. 2009; Reynaud and Ferrier-Pagès, Meistertzheim et al. (2016) also suggest differences of bacte-
this volume). There is also evidence that the seasonal spawn- rial diversity between with L. pertusa and M. oculata. Also,
ing could be triggered by phytodetrital food fall (Waller and both species have relatively few associated archaea or at least
Tyler 2005; Brooke and Jarnegren 2013; Larsson et al. 2014). rather specific groups of associated archaea compared to other
Others have shown that dissolved free amino acids can be a invertebrates for sediment and water column samples of the
significant source of carbon and nitrogen (Gori et al. 2014) same environment (Weinbauer et al., this volume).
and that L. pertusa has likely an opportunistic feeding strat- Biogeographical comparisons of bacteria associated with L.
egy (Mueller et al. 2014). In addition, both coral species pertusa have been made indicating that a core microbiome
release significant amounts of mucus into the environment exists for this species. This core microbiome of L. pertusa is
thus potentially fueling bacterial production (Reitner 2005; likely important for carbon and nutrient recycling in the mucus
Wild et al. 2008, 2010; Maier et al. 2011). Attempts have of CWCs (Kellogg et al. 2017).
been made to assess viral and microbial abundance in the Here we review data on BCC and diversity of bacteria
mucus and coelenteron of CWCs (e.g. Weinbauer et al. 2012). associated with L. pertusa and M. oculata. The term
Although it is long known that the coral mucus can harbour microenvironment will be used in the following for sediment,
large numbers of bacteria (e.g. Ducklow and Mitchell 1979), it dead corals, skeleton mucus and tissue. In addition, some
is relatively recent that bacteria have been investigated in more new data will be presented.
detail. For example, a large diversity of Bacteria and Archaea
in the surface mucus layer of tropical corals has been demon-
strated (Rohwer et al. 2002; Kellogg 2004; Ritchie and Smith 33.2 E
ffect of Sampling Strategies
2004; Bourne and Munn 2005; Weinbauer et al., this volume). for Assessing Bacterial Community
Bacterial communities within the surface layers of hard corals Composition and Diversity
have been shown to play an important nutritional role for cor-
als (and other invertebrates) (e.g. Neave et al. 2017; Silveira It has been argued that the technology used to collect CWCs
et al. 2017); they may play an equally important role in main- such trawls, nets, dredges, box cores and remotely operated
taining the health and preventing disease in corals (Ritchie and vehicles (ROVs) could influence the outcome of studies on
Smith 2004). There is evidence that bacteria associated to microbial diversity. Potential cross-contamination could
coral mucus produce antibiotics as defense mechanisms occur between coral specimens kept in the same container.
against free-living bacteria including potential pathogens Probably more important, the contact with sediment, inverte-
(Harder et al. 2003; Ritchie 2006). It has also been suggested brates, mobile fauna, or water masses between the collection
recently that associated bacteria (including those in the tissue) point and the retrieval at the surface could contaminate the
function as an equivalent to an immune system (coral probi- coral samples (e.g. Kellogg et al. 2009).
otic hypothesis) (Reshef et al. 2006). In addition, it has been Sampling strategies were tested with Lophelia pertusa
argued that the prokaryotic community could be a way for the from the Mingulay Reef (Großkurth 2007).1 While dead
holobiont to counteract environmental disturbances such as corals, mucus and tissue clustered well apart using cluster
those caused by climate change (Rosenberg et al. 2007). analysis, as long as ‘clean’, i.e. not contaminated looking
Previous work indicated that the coral microbiome can be con- colonies were used (see also next section: Community
ceptually divided into three components: (i) a small ubiquitous
core microbial (mutualists and symbionts), (ii) a dynamic site Masters thesis available as pdf at [email protected]
1
33 Diversity of Bacteria Associated with the Cold Water Corals 379
Composition and Diversity of Bacteria Associated with intensity or peak height) rather than as differences in bacterial
Coral Mucus and Tissue), no consistent effect on BCC were OTUs (Terminal Restriction Fragment Length Polymorphism,
found for the sampling devices box core and videograb. An T-RFLP analysis) between pink and white colonies
exception was dredged samples which clustered together (Neulinger et al. 2008). Using ARISA, Schöttner et al. (2012)
with dead corals. This suggests that sampling strategies do found no significant differences between color morphs, as
not have a strong influence as long as colonies with visible observed for pyrosequencing in Meistertzheim et al. (2016).
contamination are not used. It is possible that the small differences between color morphs
found by Neulinger et al. (2009) were due to intracolony and
local between colony differences (e.g. Hansson et al. 2009;
33.3 Community Composition Meistertzheim et al. 2016).
and Diversity of Bacteria Associated
with Coral Mucus and Tissue
33.4.2 Sequence Analysis at the OTU Level
It has been reported for the North Atlantic that BCC differs
between Lophelia pertusa microenvironments such as skele- Most of the sequences obtained in the literature were close to
ton and mucus (Schöttner et al. 2009, 2012; van Bleisweijk bacterial sequences found to be associated to (tropical) corals
et al. 2015). For example, the number of Automated and sponges (Neulinger et al. 2008, 2009; Kellogg et al.
Ribosomal Intergenic Spacer Analysis (ARISA) Operational 2009, 2017; van Bleijsweijk et al. 2015; Meistertzheim et al.
Taxonomic Unit (OTUs) was lower for the skeleton (7) than 2016). Potentially these bacteria are the result of the
for mucus (14) (Schöttner et al. 2009). Using Denaturing diversification of specific groups of bacteria that are adapted
Gradient Gel electrophoresis (DGGE, Großkurth (2007) to corals and sponges.
found for L. pertusa that dead corals, mucus and tissue typi- A “symbiontlike thiotrophs cluster” (including uncul-
cally showed distinct clusters as long as mucus and tissue was tured bacterium clone G02_CR02) was found in the Gulf of
collected from not contaminated looking corals. This author Mexico and North West Atlantic (Kellogg et al. 2009), the
also showed that (1) rinsing of contaminated looking corals Trondheimsfjord (Neulinger et al. 2008), Rockall Bank,
resulted in a re-clustering of samples into the ‘typical’ micro- Mingulay Reef and the Apulian Platform (this study,
environment and (2) rinsing of not contaminated looking cor- Table 33.2). This indicates a biogeographical constancy of
als resulted in only minor changes of BCC. this phylotype between Gulf of Mexico, North Atlantic and
The detailed reasons for the difference between microen- Mediterranean Sea. These sequences are of particular inter-
vironments remain unknown, however, it has been demon- est because they are part of what represents one of the
strated before that specific bacterial groups can invade potential Lophelia-specific bacterial groups (Kellogg et al.
different tissues of tropical corals (Ainsworth et al. 2006). 2009).
Other bacteria could have a life strategy to become embedded Two phylotypes within the Gammaproteobacteria
in the organic matrix of the mucus as shown for marine (including uncultured bacterium clone G02_CR02) were
organic aggregates (Heissenberger et al. 1996). For tropical most closely related to endosymbionts of deep-sea mussels
corals it has been suggested that it is the tissue that harbors colonising hydrothermal vents (Neulinger et al. 2008). They
the core microbiome (Hernandez-Agreda et al. 2017). might utilise reduced sulphur compounds produced by
Overall, mucus, tissue and skeleton are quite different and decomposition of Dimethylsulfonioproprionate (DMSP).
specific microenvironments hence, likely providing Hence, it has been speculated that metabolising sulphur
ecological niches for specific bacteria. compounds is important in CWCs (Neulinger et al. 2008).
Raina et al. (2009) suggested that DMSP, DMS, and acrylic
acid potentially act as nutrient sources for coral-associated
33.4 Community Composition bacteria (Montipora aequituberculata and Acropora mille-
and Diversity of Bacteria Associated pora). Such sequences were also found at Rockall Bank,
with Lophelia pertusa Mingulay Reef and the Apulian Platform (this study,
Table 33.2).
33.4.1 Number of OTUs Sequences related to Mycoplasma spp. and the TMF7
(including uncultured bacterium clone D11_CW02) were
A literature survey shows that 14–36 OTUs were found using found in the North East and North West Atlantic (Neulinger
various fingerprinting techniques, 12–79 using clone libraries et al. 2008, 2009; Kellogg et al. 2009) and are now also
and 2–1761 using in-depth sequencing (Table 33.1). reported for other Atlantic environments (Rockall and
Specific coral-color dependent bacterial consortia were Mingulay Reef) and for the Mediterranean Sea by a DGGE
discovered as differences in relative abundance (band approach (this study, Table 33.2) but not by pyrosequencing
Table 33.1 Data compilation from the literature of bacterial diversity associated with the mucus of Lophelia pertusa. Only phylogenetic groups
with a representation of more than 10% were considered
Depth No. of Major phylogenetic groups

Environment (m) T (°C) OTUs % Group Method References
Mediterranean Sea
Apulian plateau 784 12 55 Acidobacteria rDNA clone
library
25 Nitrospira
19 Proteobacteria
12 Alphaproteobacteria
561–625 13.8 2.6 100 Gammaproteobacteria DGGE Weinbauer et al. (this
volume)
158 52 Betaproteobacteria Pyrosequencing
37 Gammaproteobacteria
Lacaze-Duthier 520 13 2–18 79–92 Alphaproteobacteria Pyrosequencing
canyon
6–78 Gammaproteobacteria
26–42 Fusobacteria
31–37 Bacteroidetes
NE Atlantic
Trondheimsfjord 54 9.6 27–54 28–61 Alphaproteobacteria DNA clone library Neulinger et al. (2009)
19 Actinobacteria
Langenuen fjord 167 14 ARISA Schöttner et al. (2009)
Norwegian fjords 300–400 36 ARISA Schöttner et al. (2012)
Rockall Bank 528–745 5.4–10.0 1761 49 Gammaproteobacteria Amplicon
sequencing
558–781 8.5 7.4 49–60 Alphaproteobacteria DGGE Weinbauer et al. (this
volume)
0–25 Actinobacteria
0–13 Deltaproteobacteria
70 78 Gammaproteobacteria Pyrosequencing
17 Betaproteobacteria
Mingulay reef 129–179 9.9 8.1 58 Alphaproteobacteria DGGE Weinbauer et al. (this
volume)
14 Firmicutes
NW Atlantic
Gulf of Mexico 315–500 7–13 79 52 Tenericutes DNA clone library Kellogg et al. (2009)
397–543 8.2-10.0 33 Gammaproteobacteria
Atlantic 743–751 8 94–712 >80 Proteobacteria Pyrosequencing Kellogg et al. (2017)
For the Weinbauer et al. (this volume) samples, DNA extraction, DGGE and sequencing of bands was done as in Großkurth (2007) and Hansson
et al. (2009) and pyrosesquencing for pooled samples (same DNA amount per specimen) as in Ray et al. (2012) and An et al. (2013). For Weinbauer
et al. (this volume): n = 3 for the Apulian Plateau, n = 9 for Rockall Bank and n = 10 for Mingulay Reef
(Meistertzheim et al. 2016). Pyrosequencing did also not Mycoplasma. Using a single cell detection approach and
result in Mycoplasma related sequences at Rockall Bank microscopy (fluorescence in situ hybridisation, FISH),
(van Bleisweijk et al. 2015). Kellogg et al. (2017) who Mycoplasma was detected in the tissue of L. pertusa
found such Tenericutes OTUs by pyrosequencing suggest (Neulinger et al. 2009). Thus, it is also possible that
that this could be due to the higher sequencing depth of Mycoplasma is not detected when only mucus is sampled
their study. Also, it is possible that pyrosequencing selects (Kellogg et al. 2017). However, Meistertzheim et al. (2016)
against Mycoplasma and/or that DGGE selects for did not detect Mycoplasma when sampling tissue within
Table 33.2 Data compilation from the literature of bacterial diversity associated with the mucus of Madrepora oculata
Major phylogenetic groups
Environment Depth (m) T (°C) No. of OTUs % Group Method References
Mediterranean Sea
Lacaze-Duthier canyon 520 13 4–28 74–99 Gammaproteobacteria Pyrosequening Meistertzheim et al. (2016)
12–16 Alphaproteobacteria
Apulian platform 561–625 13.8 10.3 33 Bacteroidetes DGGE Weinbauer et al. (this volume)
33 Deltaproteobacteria
33 Diversity of Bacteria Associated with the Cold Water Corals
NE Atlantic
Rockall Bank 558–781 8.5 6–10 81 Gammaproteobacteria DGGE Hansson et al. (2009)
13 Actinobacteria
5.6 80–87 Gammaproteobacteria DGGE Weinbauer et al. (this volume)
Norwegian fjords 300–400 35 ARISA Schöttner et al. (2012)
Only phylogenetic groups with a representation of more than 10% were considered. For the Weinbauer et al. (this volume) samples, DNA extraction, DGGE and sequencing of bands was done as
in Hansson et al. (2009) and pyrosequencing for pooled samples (same DNA amount per specimen) as in Ray et al. (2012) and An et al. (2013). For Weinbauer et al. (this volume): n = 3 for the
Apulian Plateau and n = 18 for Rockall Bank
381
polyps. Hence, the presence of Mycoplasma in L. pertusa 33.5.2 Sequence Analysis at the OTU Level
remains enigmatic.
Using next-generation data sets, Proprionibacterium was Similar to Lophelia pertusa, most sequences of Madrepora
detected on L. pertusa in the Gulf of Mexico, the NW oculata were related to bacteria associated with (tropical)
Atlantic (Kellogg et al. 2017), the NE Atlantic (van corals and sponges (Hansson et al. 2009; Schöttner et al.
Bleijsweijk et al. 2015) and the Mediterranean Sea 2012; Meistertzheim et al. 2016).
(Meistertzheim et al. 2016). This suggests that some bacte- Several sequenced DGGE bands from Mingulay Reef had
rial phylotypes are conserved regardless of geographic prov- a close similarity to Endozoicomonas; also a high sequence
enance (Kellogg et al. (2017). variability within the genus was detected (Hansson et al.
2009). Such DGGE sequences were also found for Rockall
Bank and the Apulian platform (this study, Table 33.2).
33.4.3 Sequence Analysis at Higher Taxonomic Endozoicomonas-related sequences were also detected in the
Levels Mediterranean Sea (Meistertzheim et al. 2016). This further
suggests specific associations of Endozoicomonas with M.
A high relative contribution of Gammaproteobacteria (75%) oculata. Genomic analyses indicate that Endozoicomonas is
was found by Yakimov et al. (2005) associated to dead a symbiotic bacterium with high genetic and metabolic plas-
Mediterranean L. pertusa, while in living L. pertusa from the ticity (Neave et al. 2017).
Apulian Plateau, the most abundant phylotypes were Endozoicomonas sequences have been observed previ-
Holophaga acidobacteria and Nitrospirae. Sequencing of ously as dominating a culture-independent assessment of
DGGE bands revealed only Gammaproteobacteria sequences Acropora millepora at Magnetic Island (Bourne et al. 2008).
at the Apulian Plateau; this study and all previous ones suggest Bourne et al. (2008) showed that Endozoicomonas-related
that Gammproteobacteria are abundant in L. pertusa from all sequences dominated bacterial profiles before and after a
sites studied so far (Table 33.1). One of the reasons for the dif- bleaching event, but were not dominant during the stress
ferences for Gammaproteobacteria compared to the study of period. The high diversity of 16S rRNA gene sequences of
Yakimov et al. (2005) could be that an RNA based clone Endozoicomonas suggests adaptive radiation in M. oculata
library was used as an indicator for active bacterial members. (Hansson et al. 2009). Littman et al. (2009) demonstrated
If this finding holds, this means that Gammaproteobacteria that Endozoicomonas-related sequences accounted for
are less active than other bacteria in L. pertusa. 17–35% of acroporid corals of the Great Barrier Australian
Reef. Being such a dominant member of the coral-associated
microbial communities could indicate that Endozoicomonas
33.5 Community Composition plays also a key role in the M. oculata holobiont system.
and Diversity of Bacteria Associated
with Madrepora oculata
33.5.3 Sequence Analysis at Higher Taxonomic
33.5.1 Number of OTUs Levels
A literature survey shows that between 6 and 35 OTUs were A literature survey suggests that Gammaproteobacteria are a
found by fingerprinting techniques and between 4 and 138 significant and often dominating group of bacteria for M.
OTUs by pyrosequencing (Table 33.3). oculata (Table 33.3).
Table 33.3 Phylogenetic affiliation of sequences from DGGE bands with closest uncultured matches for Lophelia pertusa and Madrepora ocu-
lata from this study
Bacterial group Closest relative (data base accession no) Similarity (%) Affiliation
L. pertusa
Symbiontlike thiotrophs cluster Uncultured bacterium clone G02_CR02 (AM911391) 100 Gammaproteobacteria
Uncult.bact.envir.samp. (AB254034) 100 Gammaproteobacteria
Mycoplasma spp. Uncultured bacterium clone D11_CW02 (AM911412) 100 Firmicutes
M. oculata
Endozoicomonas uncultured Spongiobacter sp. (DQ917863) 97 Gammaproteobacteria
uncultured Spongiobacter sp. (DQ889928) 95 Gammaproteobacteria
Spongiobacter nickelotolerans (AB205011) 97 Gammaproteobacteria
The number of bases used to calculate sequence similarity ranged from 446 to 502. Identical DGGE bands for these sequences were obtained from
the Apulian Plateau, Rockall Bank and Mingulay Reef
33.6 C
omparison of Bacterial Diversity it was shown that the genetic structure of L. pertusa differed
Associated with Lophelia pertusa between continental margins, offshore banks and fjords in
and Madrepora oculata the NE Atlantic (Le Goff-Vitry et al. 2004; Boavida et al.,
this volume). These factors could contribute to the finding of
Schöttner et al. (2012) using a high resolution method different bacterial communities associated with L. pertusa
(ARISA) did not find any significant difference between the and M. oculata.
two species (Table 33.1). On the contrary, differences
between the two species were also found in previous studies
comparing specimen from the same environment (Hansson 33.7 Spatial Variability
et al. 2009; Schöttner et al. 2012; Meistertzheim et al. 2016).
As discussed above, several potential mutualists for Lophelia Comparative analysis of Lophelia pertusa derived 16S rRNA
pertusa (e.g. Neulinger et al. 2008, 2009; Kellogg et al. 2009, gene sequences from different areas showed that with the
2017) and one potential mutualist for Madrepora oculata exception of potential mutualists, Mediterranean L. pertusa
(Hansson et al. 2009) were detected in the Atlantic and the hosted bacterial phylotypes (Yakimov et al. 2005) that were
Mediterranean Sea. This reinforces the idea that these bacte- almost completely different from those in Norwegian
rial phylotypes are indeed constantly associated with specific specimens (Neulinger et al. 2008). As discussed above, one
corals. The finding that Endozoicomonas is associated to of the reasons for that could be that L. pertusa has been
many tropical corals and sponges in general as well as to M. described as a rather opportunistic species with respect to
oculata but rarely to L. pertusa suggests that even corals liv- associated bacteria, whereas for Madrepora oculata the host
ing in the same environment can develop quite variable evo- influence could be stronger (Meistertzheim et al. 2016). The
lutionary solutions. spatial differences of bacterial communities could also be
In a study in the Mediterranean Sea, where both corals due to different biotic or/and abiotic environmental factors
species occurred in the same environment, M. oculata was between the two areas. For example, in the North Atlantic L.
dominated by Gammaproteobacteria and L. pertusa by pertusa occurs preferentially at a salinity of 32–38.8 and a
Alphaproteobacteria (Meistertzheim et al. 2016). At Rockall temperature from 4 to 13 °C (Roberts et al. 2006; Dodds
Bank and at the Apulian Plateau samples were collected et al. 2007). At Rockall Bank temperature is 6.6–10 °C and
from both species. Differences between the two species at salinity ca. 35.5 (van Bleijsweijk 2015), whereas temperature
the class level (assessed from sequenced DGGE bands) were was 9.4–10.4 °C and salinity 35.5 at the Mingulay Reef (this
detected in both environments. At Rockall Bank L. pertusa study). Samples of L. pertusa from Norwegian CWC reefs
was dominated by Gammaproteobacteria and M. oculata by were sampled at 8.8 °C and 30.8 (Neulinger et al. 2008).
Alphaproteobacteria. At the Apulian Plateau L. pertusa was Differences could be due to variations in physicochemical
dominated by Bacteroidetes and Deltaproteobacteria and for factors between the two areas. Yakimov et al. (2005) found
M. oculata only Gammaproteobacteria were found (this that most deep-water scleractinians collected from the
study) (Tables 33.1 and 33.2). Mediterranean were dead and covered by Fe–Mn oxides. It
From studies in the field of microbial ecology of warm has been suggested that the relatively limited occurrence of
water corals, it is long known that coral-associated microbes living corals in the Mediterranean Sea compared to the
appear to be coral species-specific (e.g. Kuhl et al. 1995; Atlantic is a consequence of the high temperature and salinity
Santavy 1995; Rohwer et al. 2001, 2002; Knowlton and in deep waters (12.7–14.5 °C, salinity 38.4–39.0) (Taviani
Rohwer 2003) as now seen in the sense of a core microbiome et al. 2005; this study). This temperature seems to be at the
(Fernandez-Agreda et al. 2016, 2017). upper limit of the thermal tolerance of this species (e.g.
Lophelia pertusa seems to be a more opportunistic spe- Maier et al., this volume).
cies than M. oculata, both in feeding strategies (Mueller Environmental factors could also explain the band vari-
et al. 2014) and associated bacteria (Meistertzheim et al. ability (band number and pattern) and sequence variability at
2016). Also, there are potential differences in the uptake of a local scale as reported before for L. pertusa (Groβkurt
dissolved free amino acids by mucus bacteria (Gori et al. 2007; Meistertzheim et al. 2016) and M. oculata (Hansson
2014) and in the composition of mucus (Wild et al. 2010). et al. 2009; Meistertzheim et al. 2016). Localised circulation
The two coral species might have a different temperature tol- patterns due to the 3D structure of the reef, presence of
erance (e.g. Naumann et al. 2014; Maier et al., this volume; slopes resulting in differences of the support of nutrition,
Movilla, this volume; Reynaud and Ferrier-Pagès, this vol- daily variations of temperature and salinity could affect the
ume) and this could influence the microbiome. In addition, physiology of corals, hence the coral associated bacteria (van
genetic differences between coral populations in the same Bleijsweijk et al. 2015). At Rockall Bank, temperature
environment could influence bacterial diversity. For example, showed a prominent and relatively large daily variation of ca.
2 °C reflecting the alternation of deep cold water flowing across ocean level, and this could also partly explain
upslope and warmer water flowing downslope (see also van differences between studies. Concepts such as the three
Bleijsweijk et al. 2015). At Mingulay Reef temperature vari- components model of the coral microbiome (Hernandez-
ations of 0.75 °C were observed within 3 h and the hydro- Agreda et al. 2017) represent a framework for better
graphic environment such as downwelling and bottom understanding CWCs. However, there are also other
currents shape the food supply (Davies et al. 2009; Roberts potentially useful (ecological) concepts such as the
et al. 2009; Findlay et al. 2013). This could result in a varia- metacommunity theory. This concept is an important way to
tion of the food sources for the corals and thus, influence think about linkages between different spatial scales in
their metabolism. It is possible that different environmental ecology. A metacommunity can be defined as a set of local
parameters of the sampled area could affect the diversity of communities that are linked by dispersal of multiple
the bacteria consortia associated to the corals. potentially interacting species (Leibold et al. 2004). Applied
Biogeographical constancy of certain bacterial groups to specific bacterial types associated with CWCs, one could
was reported using DGGE fingerprinting of three different argue within the framework of this concept that the dispersal
acroporid corals species of two different areas in the Great of bacteria released from or with mucus from corals and the
Barrier Reef (Magnetic island and Orpheus island) separated colonisation of other coral specimen contributes to and
by 40 km (Littman et al. 2009). The biogeographical sustains the bacterial diversity of CWCs at least the site-
constancy of certain bacterial groups was cross-validated by specific and/or species-specific community and the highly
T-RFLP and clone libraries analyses. Nonetheless the variable community influenced by abiotic and biotic factors
numbers of non-shared bacterial groups were conspicuous, in the sense of Hernandez-Agueda et al. (2016).
indicating geographic separation of coral associated bacteria Overall, these findings indicate that in-depth studies of
separated only even by 40 km (Littman et al. 2009). Previous the role of specific bacteria for the functioning of the coral
studies have reported that similar bacterial populations have holobiont constitute a reasonable quest in CWC research. M.
been found on the same coral species that are geographically oculata has received less attention than L. pertusa and other
separated (Rohwer et al. 2001, 2002), suggesting that corals scleractinians or gorgonians remain even less studied. Such
associate with certain bacteria despite geographic separation. research is also warranted considering that CWCs are host
One prerequisite to call an observed coral-microbe asso- spots for marine diversity and breeding ground or habitat for
ciation truly “specific” is biogeographical constancy fishes and crabs and that they are threatened by fisheries, oil
(Neulinger et al. 2008). Schöttner et al. (2012) found that and gas prospecting, global warming and OA.
habitat was the main structuring factor for bacterial diversity
associated with CWCs. Coral mucus could trap particles and Acknowledgements We thank the captain and the crew of the RVs
microbes that pass by in the water column (Wild et al. 2004), Pelagia and Thethys I’ for their support, as well as the supporting
departments at NIOZ for coordination, data management and technical
thus, many microbes trapped in coral mucus are less likely to support. This research has been financed by the Dutch NWO/ALW
be true ‘residents’, but rather ‘visitors’ consisting of transient project BIOSYS (no. 835.30.024 and 814.01.005) and the project
commensal microorganisms (that do no good or harm), or COMP of the Foundation Prince Albert II (Monaco). This work is also
organisms that can potentially become opportunistic under a contribution to the ‘European Project on Ocean Acidification’
(EPOCA) which received funding from the European Community’s
appropriate conditions (Ritchie and Smith 1995). A large Seventh Framework Specific Programme (PP7/2007-2013) under grant
bacterial local variability within Mingulay L. pertusa was agreement no. 211384.
observed by Großkurth (2007). Band variability within areas
could be due to fluctuations of local flora and fauna (Ritchie
and Smith 1995). Another reason could be related to the
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Drop Chapter
Lophelia pertusa and Madrepora 34
oculata: An Archaea Riddle?
Markus G. Weinbauer, Davide Oregioni,
and Cornelia Maier
Abstract
Lophelia pertusa and Madrepora oculata are the two water column and the sediments surrounding CWCRs are
main species building cold-water coral reefs. Habitats inhabited by Archaea (Yakimov et al. 2006; Beman et al.
within cold-water coral reefs ecosystems such as the 2007; Hansson et al. 2009); also in CWCRs sponges up to
water column, sediments, coral rubble, sponges and other 30% of the prokaryotes could be affiliated to Archaea (van
corals host a diverse archaeal community. However, L. Duyl et al. 2008). Studies of prokaryotes on tropical corals
pertusa and M. oculata host, if at all, a different archaeal have revealed that Archaea can be a diverse group of micro-
community. The question arises why (some) Archaea are organisms associated with the coral holobiont, i.e. the coral
excluded from the holobiont and whether this is poten- itself plus associated microorganisms (Kellogg 2004; Wegley
tially contributing to the success of L. pertusa and M. ocu- et al. 2004). However, there is comparatively little evidence
lata as cold-water coral reef builders. of Archaea associated with the CWCs Lophelia pertusa and
Madrepora oculata as discussed below (see also Table 34.1).
In the present study, samples of L. pertusa and M. oculata
Keywords from the NE Atlantic (Rockall Bank and Mingulay reef com-
Bacteria · Archaea · Corals · Diversity · Holobiont plex) and the Mediterranean Sea (Apulian plateau) were
investigated to assess the presence of Archaea in the mucus
and whole coral microhabitats. The DNA extraction and
PCR approach was the same as used in Hansson et al. (2009)
In the water column of the oceans, the relative amount of and Weinbauer et al. (this volume). The archaeal primers
Archaea increases with water depth and reaches roughly 344F-GC/915R targeting a 16S rRNA gene fragment, were
equivalent numbers compared to Bacteria in the mesope- used with the intention to perform denaturing gradient gel
lagic zone of the ocean, i.e. the twilight zone between about electrophoresis (DGGE) fingerprints. However, no amplifi-
200 and 1000 m where the light intensity is too low for sus- cation products were obtained from any of the investigated
taining photosynthesis. This increase of archaeal abundance samples (control samples from mesopelagic water revealed
is due to the phylum Crenarchaeota (now termed PCR products). The DNA was extracted from these samples
Thaumarcheota), whereas the relative abundance of the phy- with a simplified extraction method based on heat and salt
lum Euryarchaeota remains roughly constant (e.g., Fuhrman treatment (HEATSALT method), thus, this extraction could
et al. 1992; Massana et al. 1997; Fuhrman and Ouverney be biased against Archaea. However, an extraction method
1998; Delong and Pace 2001; Delong et al. 1994; Vetriani involving repeated freeze-thawing cycles, proteinase
et al. 1999; Karner et al. 2001). The mesopelagic zone is also K-lysozyme digestion and phenol-chloroform extraction and
the habitat of many cold-water coral reefs (CWCRs). The the same primers also did not result in a positive PCR prod-
uct for Archaea (Hansson et al. 2009). Further, PCR products
were obtained for Bacteria in these samples and the amount
of PCR product and the number of DGGE products was not
M. G. Weinbauer (*) · D. Oregioni · C. Maier systematically different between extraction methods. In
Sorbonne Universités, CNRS, Laboratoire d’Océanographie de
Villefranche, Villefranche-sur-Mer, France addition, there was no difference in the amount of PCR prod-
e-mail: [email protected] ucts and the number of DGGE bands between the two DNA

https://doi.org/10.1007/978-3-319-91608-8_34
Table 34.1 Compilation of studies attempting to detect Archaea in the cold water corals Lophelia pertusa and Madrepora oculata
Presence/
Species Environment/habitat Methods absence Type Reference
L. pertusa Med Sea, Apulia cr clone library – NA Yakimov et al.
plateau (2006)
L. pertusa + M. oculata NE Atlantic, Rock 16S rRNA PCR – NA Hansson et al. (2009)
Bank
L. pertusa + M. oculata NE Atlantic, Med 16S rRNA PCR – NA This study
Sea
L. pertusa + M. oculata NE Atlantic, CARD-FISH + 0.9% vs 3% Unpublished
Rockall Bank
L. pertusa Nord-Leska, 454 sequencing + Nitrosopumilus, Nitrosoarchaeum, Emblem et al. (2012)
Norway Cenarchaeum
L. pertusa NE Atlantic, 454 sequencing + 11% Thaumarchaeota marine class van Bleijsweijk et al.
Rockall Bank I and 0.5% Euryarchaeota (2015)
For details of methods see Weinbauer et al. this volume (full chapter) and Hansson et al. (2009)
NA: not applicable
extraction methods for mesopelagic water samples from the However, data on autofluorescence which could interfere
Mediterranean Sea (Hansson et al. 2009). Also, no archaeal with the CARD-FISH approach do not allow for a defini-
DNA PCR product was obtained when DNA was extracted tive proof of the presence of Archaea for L. pertusa and M.
from corals using a soil extraction kit (Weinbauer et al. oculata, whereas the archaeal counts for other corals and
unpublished data). It is worthwhile mentioning that the used for sponges from the CWCR were higher than the detect-
primers are more specific for Euryarchaeota than for able autofluorescence (Weinbauer et al. in preparation).
Crenarchaeota (Winter et al. 2009). However, using the Using 454 sequencing, archaeal sequences (11%
above mentioned primers, archaeal PCR products were Thaumarchaeota marine class I and 0.5% Euryarchaeota)
obtained for some sponges (the hexactinellidan sponge were detected in the mucus of L. pertusa (van Bleijsweijk
Rossella nodastrella and the demosponges Hexadella et al. 2015). In addition, a sequence covering 60% of the
dedritifera, Higginsia thielei and Tentorium semisuberites), whole genome of an archaeon was detected in L. pertusa
the solitary stony coral Desmophyllum sp., the gorgonian (Emblem et al. 2012). The possibility of contamination
coral genus Paramuricea and an unidentified antipatharian from ambient water or sediments during sampling cannot
coral from the Rockall Bank CWCR study area (Weinbauer be fully excluded. However, as more than 10% of the
et al. unpublished data). sequences were affiliated with Archaea, this seems unlikely.
Using another method, i.e. a DNA library targeting 16S The in-depth sequencing suggests that Archaea are pres-
rRNA transcripts, no archaeal PCR products could be ent in L. pertusa, however, the lack of positive sequences
detected from metabolically active microbial communities using other primers or probes and the cr clone library indi-
(as assessed by targeting rRNA) associated with the deep cate that these Archaea represent poorly studied (e.g. not
water coral L. pertusa from the Apulian plateau detected by all primers) or metabolically not active phylo-
(Mediterranean Sea; Yakimov et al. 2006). Primers target- types. This compilation of data supports the idea that L. per-
ing the marker gene accC encoding the biotin carboxylase tusa and M. oculata specifically exclude (at least some)
gene subunit (biotin carboxylase) from Atlantic and Archaea compared to the water column, sediment, sponges
Mediterranean coral samples revealed PCR products and and some other corals in CWCRs. Also, the idea can be put
sequencing of bands from genetic fingerprints (DGGE) was forward that this feature could be linked to the reef forming
used to potentially detect Archaea and Bacteria. The capacity of L. pertusa and M. oculata. As Archaea are plenti-
sequences were only related to Bacteria and bacterial ful in tropical hermatypic corals (Kellogg 2004; Wegley
sequences were similar to the phylotypes obtained from et al. 2004), this suggests that Archaea-coral associations (or
16S rRNA-based sequences; no Archaea were detected. the lack of them) in CWCR are ecosystem-specific. Indeed,
Using Catalysed Reporter Deposition–Fluorescence In situ archaeal diversity was only habitat-specific in the mucus of
Hybridisation (CARD-FISH), i.e. a single cell based analy- Caribbean corals, whereas bacterial diversity was influenced
sis, ≤3% of prokaryotic abundance was due to Archaea on. by habitat, coral species and spatial distance (Frade et al.
L. pertusa (0.9%) and M. oculata (3%) in samples from 2016). The reasons could be linked to differences in tem-
Rockall Bank, whereas, for the same CWCR environment, perature or lack of photosynthesis, however, this remain
9% of the prokaryotes were Archaea on Paramuricea sp., unknown. As habitat-specificity seems unlikely –in contrast
8% on Desmophyllum sp. and between 5% and 11% on to tropical corals (Glasl et al. 2017) –species-specific asso-
various sponge species (same species as mentioned above). ciations seem possible. Considering the high abundance of
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Massana R, Murray AE, Preston CM, et al (1997) Vertical distribution
Pelagia for their support. This research has been supported by the
and phylogenetic characterization of marine planktonic archaea in
Dutch NWO/ALW project BIOSYS (no. 835.30.024 and 814.01.005)
the Santa Barbara channel. Appl Environ Microbiol 63:50–56
and the European Project on Ocean Acidification (EPOCA) which
van Bleijsweijk JDL, Whalen C, Duineveld GCA, et al (2015) Microbial
received funding from the European Community’s Seventh Framework
assemblages on a cold-water coral mound at the SE Rockall Bank
Programme (PP7/2007-2013) under grant agreement no. 211384.
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Biology and Ecophysiology
of Mediterranean Cold–Water Corals 35
Stéphanie Reynaud and Christine Ferrier-Pagès
Abstract depth, large reefs have also been observed in the

Cold-water coral ecosystems represent an important and Mediterranean Sea, where they prosper between 150 and
diverse benthic community in the Mediterranean Sea. 1200 m (e.g. Zibrowius 1980; Tursi et al. 2004; Taviani et al.
Although the distribution of cold-water corals, as well as 2005; Freiwald et al. 2009; Orejas et al. 2009; Mastrototaro
their diversity, has started to be well studied, little is et al. 2010; Addamo et al. 2012; Gori et al. 2013; Savini et al.
known about the effects of environmental changes on the 2014; Altuna and Poliseno, this volume; Chimienti et al., this
physiology of these corals. This chapter presents the state volume).
of knowledge on the rates of calcification, respiration, Scleractinian deep-sea corals, often referred as cold-water
feeding, mucus production and reproduction of the differ- corals (CWC), are the main reef builders in the deep ocean
ent Mediterranean species under their normal living con- (Freiwald et al. 2004; Baillon et al. 2012; Roberts and Cairns
ditions, and discusses the effects of climate change on the 2014). Thus, studies on their physiological traits, such as
corals’ physiology. Our review indicates the need for fur- calcification, respiration, reproduction and nutrition are of
ther investigations, especially on the calcification pro- main importance, because the growth and development of
cesses, as well as the natural food sources available in the reefs will depend on the health of their main builders. The
deep for these corals. principal human threats to the deep sea are the disposal of
wastes (structures, radioactive wastes, munitions and carbon
Keywords dioxide), fishing, oil, gas and marine mineral extraction, as
Cold water corals · Mediterranean Sea · Respiration · well as climate change (Roberts et al. 2009). CWC health is
Calcification · Reproduction · Organic matter · Global largely impacted by global change threats (Guinotte et al.
change 2006; Roberts et al. 2006), which could affect more rapidly
the Mediterranean Sea than the other oceans, due to its small
size and the expected rapid response to global change
(Bethoux et al. 1990; Coll et al. 2010; Calvo et al. 2011;
35.1 Introduction Marbà et al. 2015; Maier et al., this volume; Otero and Marin,
this volume). Large-scale warming of the Mediterranean Sea
The first observations on the distribution of coral reefs has already been observed (Walther et al. 2002; Coma et al.
performed at the beginning of the twentieth century suggested 2009; Vargas-Yáñez et al. 2010), with a 0.5 °C increase in the
that they were mostly thriving in the warm and shallow mean temperature between 1985 and 2000 (Rixen et al.
waters of tropical and subtropical regions; however, more 2005). This mini-ocean is also threatened by seawater
recent investigations, which used advanced technologies, acidification (Orr et al. 2005), which has decreased seawater
have discovered large coral reefs in the dark, cold, and nutri- pH by 0.05–0.14 pH units since pre-industrial times
ent-rich deep waters of all world’s oceans. While most expe- (Touratier and Goyet 2011), especially in deep waters where
ditions have been carried out on cold-water reefs of high the pH change is estimated to be between −0.005 and −0.086
latitudes (Freiwald et al. 2004), thriving from 40 to 4000 m pH units (Orr et al. 2005; Guinotte et al. 2006; Palmieri et al.
2015). Human-induced global changes have been recognised
S. Reynaud (*) · C. Ferrier-Pagès as main threats to corals in general, whose calcification,
Département de Biologie Marine, Equipe d’Ecophysiologie, among others, is affected both by increased temperature and
Centre Scientifique de Monaco, Monaco, Monaco
e-mail: [email protected] acidification (Gattuso et al. 1998; Langdon et al. 2000;

https://doi.org/10.1007/978-3-319-91608-8_35
392 S. Reynaud and C. Ferrier-Pagès
Kleypas et al. 2006; Gazeau et al. 2007; Kuffner et al. 2007); the faculty to take up dissolved compounds indicates that
CWC are particularly sensitive to both threats (Guinotte this food source can be important when particulate food is
et al. 2006; Roberts et al. 2006; Maier et al. 2013a, b; Movilla scarce (Ambariyanto and Hoegh-Guldberg 1999; Naumann
et al. 2014a, b). A reduction in CWC distribution has thus et al. 2011; Gori et al. 2014a). Nevertheless, most studies
been observed between today and the Last Glacial period, having investigated the natural feeding behavior of CWC,
during which they were more abundant in continental either using the nitrogen and carbon isotopic signature
margins and seamounts (Delibrias and Taviani 1985; Di (Carlier et al. 2009), the fatty acid-lipid composition of prey
Geronimo et al. 2005; Wienberg et al. 2010; Vertino et al. and coral tissue (Dodds et al. 2009; Naumann et al. 2015), or
2014, this volume; Taviani et al., this volume; other chapters the prey capture rate (Purser et al. 2010; Tsounis et al. 2010;
from the «Past» section of this volume). There is thus an Orejas et al. 2016), have shown that zooplankton was the
urgent need to investigate which are the best conditions for preferred food of Mediterranean and Atlantic CWC. However,
CWC growth and how they respond to changes in their a study performed on L. pertusa using 15N and 13C-labeled
environment. CWC physiology has been much less studied prey demonstrated that this CWC species can have an
than tropical species, owing to the difficulty in accessing opportunistic feeding strategy according to the external food
their habitats and maintaining them for laboratory studies. source (Mueller et al. 2014).
The physico-chemical conditions which favor CWC growth The CWC thus often concentrate on ridges where strong
are thus not well-known; however, several factors, such as currents enhance food accessibility (Thiem et al. 2006;
the hydrographic conditions and the reef geomorphology, Davies et al. 2009; Roberts et al. 2009). As such, capture
combined to other key environmental parameters such as rates depend on water flow (Purser et al. 2010, 2014; Gori
temperature (Frederiksen et al. 1992; Freiwald et al. 2009; et al. 2015; Orejas et al. 2016), which is a primary factor
Davies et al. 2009; Roberts et al. 2009; Orejas et al. 2011a; affecting feeding success of passive suspension feeders
Naumann et al. 2013, 2014; Gori et al. 2014a) and nutrient (LaBarbera 1984; Shimeta and Jumars 1991; Shimeta and
supply (Mortensen et al. 2001; Roberts et al. 2009; Gori Koehl 1997; Wildish and Kristmanson 1997; Wijgerde et al.
et al. 2015; Orejas et al. 2016) are of major importance for 2012). High flow speeds (10–16 cm s−1) increase prey
CWC growth. We propose here to review the existing encounter and thus prey capture rates (Fabricius et al. 1995;
knowledge on calcification, respiration, organic matter (OM) Sebens et al. 1998; Gori et al. 2015), although they can also
release, feeding rate and reproduction, and how the climate distort coral polyps, reducing their exposed surface area
changes influences scleractinian CWC physiology. (Purser et al. 2010; Wijgerde et al. 2012; Gori et al. 2015;
Orejas et al. 2016) and the efficiency of nematocysts at
holding preys (Sebens et al. 1998). Therefore, an optimal
35.2 E
nvironmental Effects on Feeding flow speed is specific for each coral species. For example,
Rates zooplankton capture efficiency of L. pertusa decreases from
low (1 and 2.5 cm s−1) to high (10 cm s−1) flow speed (Purser
Food availability is an important factor controlling coral et al. 2010; Tsounis et al. 2010; Orejas et al. 2016), due to the
health, because corals need food to survive, as well as to fact that L. pertusa, which builds complex three-dimensional
increase their tissue and skeletal mass. In situ investigations reef structures, lives in areas exposed to high flow speed (up
and isotopes and lipid signature analyses (Duineveld et al. to 20 cm s−1), however periods with very reduced flow
2004, 2007, 2012; Kiriakoulakis et al. 2005; Carlier et al. velocities (<2 cm s−1) are often associated with tides (Davies
2009; Dodds et al. 2009), as well as experiments performed et al. 2009). On the other hand, capture rates of
under laboratory conditions (Mortensen 2001; Roberts and mesozooplankton by D. cornigera are constant over a wide
Anderson 2002; Purser et al. 2010; Tsounis et al. 2010; Gori range of flow speeds (up to 10 cm s−1; Gori et al. 2015),
et al. 2015; Orejas et al. 2016; Orejas et al., this volume) because this species does not form, as far as it is currently
have shown that CWC can feed on a wide range of food know, any truly reef structure and has polyps directly exposed
sources, including detritus, phytoplankton and different size to flow (Le Danois 1948; Brito and Ocaña 2004; Sánchez
spectrum of zooplankton. Food particles are captured and et al. 2009). In addition, the large size of D. cornigera polyps
stuffed into the mouth by the tentacles, or are trapped in allows them to have sufficient tentacle surface exposed to
mucus and then sucked into the mouth (Yonge and Nicholls water flow even if they are partially deformed by high flow
1931; Lewis and Price 1975; Shimeta and Koehl 1997; speed. Food concentration can however mitigate the effect of
Riisgard and Larsen 2010). The most conspicuous flow, as capture rates will be positively and significantly
Mediterranean CWC (Lophelia pertusa, Madrepora oculata, correlated with prey abundance (Purser et al. 2010; Osinga
Desmophyllum dianthus, and Dendrophyllia cornigera) can et al. 2011). Finally, seawater temperature was shown to be a
also actively take up dissolved OM, such as free amino acids second major factor affecting feeding success in tropical
(DFAA) (Gori et al. 2014b). The fact that some animals have coral species (Mayor 1916; Edmondson 1928). To protect
35 Biology and Ecophysiology of Mediterranean Cold–Water Corals 393
themselves from a hot or cold shock, CWC are able to slow year−1. Other measurements performed using skeletal stable
down polyp contraction or nematocyst function, two factors isotopes of carbon and oxygen (Mikkelsen et al. 1982;
that reduce feeding rates (Johannes and Tepley 1974; Palardy Mortensen and Rapp 1998) have also resulted in variable
et al. 2005). growth rates, ranging from 6 to 25 mm year−1. These rates
Recent studies have shown that zooplankton starvation were much higher than that recently measured using staining,
induces a general decrease in CWC metabolic functions, which ranged from 3.77 to 7.5 mm year−1 for branches of L.
leading to reduced calcification and respiration rates as well pertusa deployed in situ during several months (in the Gulf
as mucus excretion (Naumann et al. 2011; Larsson et al. of Mexico: Brooke and Young 2009; in the northwestern
2013; Baussant et al. 2017). This observation, which needs Mediterranean: Lartaud et al. 2013). Food was however
to be further investigated with different coral species sampled suggested to exert a more important control than temperature
from different environments, suggest that zooplankton (Mortensen 2001; Roberts and Anderson 2002). In the
abundance plays a major role in the distribution pattern of Mediterranean Sea, only two studies have investigated the
CWC species. At the moment, there is little information on linear extension rates of two CWC species: they ranged from
the natural feeding rates of CWC; although we know they 8 to 17 mm year−1, with an addition of four polyps year−1 for
form reefs in food-rich areas (Findlay et al. 2013), information L. pertusa, and from 3 to 18 mm year−1 and five new polyps
on the nutritional needs of CWC and on the availability of year−1 for Madrepora oculata (Orejas et al. 2008, 2011a).
plankton and detrital particles in deep reef environments are
still lacking (van Oevelen et al. 2016). As food availability is
likely to vary according to locations and seasons, 35.3.2 Calcification Rates
measurements of plankton and other particle concentrations
in deep waters, on geographical and temporal scales, are also The highest calcification rates are measured for tropical
needed. Analyses of fatty acid and lipid composition of coral corals (between 0.4% and 2.3% increase day−1, Erez 1978;
tissue and potential food sources can also bring further Ferrier-Pagès et al. 2000; Reynaud et al. 2003) since
insights into the nutritional ecology of CWC (Dodds et al. calcification is enhanced by photosynthates provided by the
2009; Gori et al. 2014b; Mueller et al. 2014). Recently, the zooxanthellae, the so-called light enhanced calcification
discovery of chemoautotrophy, the nitrogen fixation and process (Goreau 1959; Allemand et al. 1998). Azooxanthellate
efficient recycling of nitrogen by bacterial community, may Mediterranean CWCs have generally lower growth rates
play a role in CWC energy intake and may be advantages compared to shallow-water zooxanthellate species (see
CWC in a dark and resources-limited conditions (Middelburg Orejas et al. 2011b).
et al. 2015; see Orejas et al., this volume). Calcification rates of the species Dendrophyllia cornigera
from the Mediterranean are consistent among studies and
vary between 0.04% day−1 and 0.06% day−1 (±0.005%)
35.3 G
rowth Rates and Environmental (Orejas et al. 2011a; Naumann et al. 2013; Gori et al. 2014a;
Response Reynaud, pers. obs.) (Fig. 35.1). M. oculata has however
twofold higher growth rates (ca. 0.11–0.12% day−1 (±0.03%)
Several factors determine the expansion of CWC reefs, such (Orejas et al. 2011a; Naumann et al. 2014), maybe due to its
as recruitment success, larval distribution, and tolerance to different shape and tissue thickness compared to D. cornigera
environmental changes. Coral growth rate is also an important (Fig. 35.1). It has indeed been hypothesised that the branching
parameter, as it concerns the deposition of the carbonate form, the high polyp density and polyp budding rate of M.
structure of the reef. It can be expressed as linear extension oculata, may favor the prey capture efficiency, the energy
rate or as calcification rate. Linear extension rate corresponds acquisition and thus, allocation to skeletal growth (Orejas
to a skeletal change in one dimension (length), while et al. 2011a). Conversely, D. cornigera, which has large
calcification rate is a change in volume and is equal to the polyps with a thick soft tissue above the skeleton, may
linear extension multiplied by the skeletal density (see allocate the acquired energy to tissue growth as observed in
Lartaud et al., this volume). tropical coral species by Anthony et al. (2002). This
“morphology hypothesis” is however not consistent with
further measurements performed with solitary corals
35.3.1 Linear Extension Rates (Desmophyllum dianthus) and branching species L. pertusa,
which presented similar growth rates: from 0.06 ± 0.03%
The first estimations for Lophelia pertusa from colonies that day−1 to 0.23 ± 0.08% day−1 for D. dianthus (Orejas et al.
had settled on telegraph cables (Duncan 1877), or growing 2011a; Naumann et al. 2013, 2014), and from 0.02 ± 0.01%
over oil platforms (Bell and Smith 1999; Gass and Roberts day−1 to 0.22 ± 0.06% day−1 for L. pertusa (Orejas et al.
2003) were unusually variable, ranging from 6 to 35 mm 2011a; Naumann et al. 2013). Another hypothesis given as
0.18
0.16
Calcification rates (% d–1)

0.14
0.12
0.10
0.08
0.06
0.04
0.02
M. oculata L. pertusa D. dianthus D. cornigera D. ramea C. smithii
Fig. 35.1 Calcification rates (% day−1) of different Mediterranean et al. 2011, 2013, 2014; Maier et al. 2012, 2013a, 2016; Gori et al.
CWC species (mean ± SE). The high values for standard errors are due 2014a; Rodolfo-Metalpa et al. 2015; Reynaud unpublished data). M.
to different techniques used to measured calcification rates (buoyant oculata: Madrepora oculata, L. pertusa: Lophelia pertusa, D. dianthus:
weight or total alkalinity anomaly), to different feeding regimes, and to Desmophyllum dianthus, D. cornigera: Dendrophyllia cornigera, D.
different culture temperatures. (Data from Orejas et al. 2011a; Naumann ramea: Dendrophyllia ramea, C. smithii: Caryophyllia smithii
an explanation of the large variation in observed calcification Marshall 2001; Previati et al. 2010; Ferrier-Pagès et al. 2012;
rates is that these rates may rather vary with the age of the Gori et al. 2014a), before showing lethal signs (Jokiel and
colony. In L. pertusa, calcification is indeed four orders of Coles 1977; Coles and Fadlallah 1991; Rodolfo-Metalpa
magnitude lower in old than in young polyps (Maier et al. et al. 2006). Physiological experiments performed under
2009; Lartaud et al. 2013; Movilla et al. 2014a), suggesting laboratory conditions have however demonstrated that some
that bulk calcification is an intermediate value of fast and Mediterranean CWC species can grow at maximal rates for
slow growth rates of young and old corallites, and temperatures well above their current natural thermal range
significantly depends on the ratio of each type of polyps in a (12–14 °C). For example, D. cornigera colonies maintained
branch. In addition, Mortensen (2001) also observed that during weeks to months at their in situ temperature of 12 °C
calcification is not a continuous process in corals, but rather grew twice to three times slower (0.061 ± 0.020% day−1)
alternates rapid growth periods (max.: 1.2 mm day−1) fol- than those maintained at 16 °C (0.116 ± 0.040% day−1, Gori
lowed by long pauses (>4 weeks) with almost no growth, et al. 2014a), or 17 °C (0.14 ± 0.07% day−1, Naumann et al.
being this periodic growth responsible for the density band 2013). The same observation was made for Dendrophyllia
in coral skeletons. Finally, the budding of new polyps could ramea, which increased its growth rates between 12 °C
also contribute to rapid vs. long pauses in the growth rate (0.021 ± 0.007% day−1) and 24 °C (0.211 ± 0.026% day−1) in
(Gateno and Rinkevich 2003; Maier et al. 2009). a 18-months experiment (Reynaud et al. unpublished data).
In the Mediterranean Sea, the distribution and growth of In addition to presenting increased growth, both
CWCs seems to be more limited by temperature than depth, Dendrophyllia species also formed new polyps, suggesting
since corals are most commonly distributed between 12.5 efficient thermal acclimatisation. Higher thermal threshold
and 14 °C, whereas they can thrive between 150 and 1100 m was also tested on D. dianthus, which showed 87 days
depth (Zibrowius 1980; Taviani et al. 2005; Freiwald et al. constant growth rate at 12 °C (in situ temperature) and 17 °C
2009; Orejas et al. 2009; Mastrototaro et al. 2010; Gori et al. (0.23 ± 0.08% day−1 vs. 0.19 ± 0.06% day−1) (Naumann
2013; Savini et al. 2014; Altuna and Poliseno, this volume; et al. 2013). However, when exposed to a longer period at
Chimienti et al., this volume). This is in agreement with the elevated temperature (8 months at 15 °C, Gori et al. 2016),
common observation that calcification of ectotherm calcification rates significantly decreased. Contrary to a
organisms (i.e. organisms whose body temperature varies thermal increase, a decrease in temperature from 12 to 8 °C,
with the surrounding temperature) is tightly controlled by or 6 °C (temperature occurring in the reefs of the North Sea
the ambient seawater temperature (Clausen and Roth 1975; and Atlantic) induced a drop in the calcification rates of
Coles and Jokiel 1977; Howe and Marshall 2002; Dodds Mediterranean colonies of L. pertusa (58%, Naumann et al.
et al. 2007; Naumann et al. 2013; Gori et al. 2014a). Above 2014), M. oculata (69%, Naumann et al. 2014), and D.
or below an optimal thermal range, many corals indeed lower cornigera (69%, Gori et al. 2014a). However, no mortality
their calcification and their polyp activity (Howe and was observed between 6–8 °C and 17 °C, suggesting that
CWC of the Mediterranean Sea have thermal thresholds environment. Nonetheless, in situ and experimental studies
higher than previously assumed (Naumann et al. 2013). all show that CWC are able to calcify at maximal rates even
Calcification rates of CWC may also be impacted by at predicted levels of increased pCO2 and normal growth
ocean acidification (OA), however, as two chapters of this temperatures. The only study combining rising temperatures
volume (Maier et al., this volume; Movilla, this volume) deal and pCO2 on D. dianthus calcification (Gori et al. 2016)
with this topic, no much detail will be offer on this aspect in showed that temperature had a greater impact than
the present chapter. Briefly, among the studies that have pH. Furthermore, a clear synergistic effect of the two
experimentally assessed CWC calcification rates under stressors was observed, resulting in a higher reduction in
different pH/pCO2 levels, seven were conducted with coral metabolism compared to thermal stress alone.
Mediterranean species. Maier et al. (2012) showed that Since temperature and pCO2 are likely to increase in
colonies of M. oculata, incubated under high pCO2 (from parallel in the future, more studies combining both stressors
404 to 867 μatm) for 24 h directly after sampling, didn’t are needed to fully understand the impact of climate change
show any change in calcification rates (0.06 ± 0.06% day−1). on CWC physiology. In addition to these physical stressors,
These rates however doubled (0.12 ± 0.06% day−1) when in the future acidified ocean there might also be a decrease of
colonies were incubated at the pre-industrial pCO2 level particulate organic matter (POM) supply to the deep-sea, due
(285 μatm), compared to the current higher level. It is to the reduction of surface primary production (Mora et al.
possible that M. oculata exhibits a nonlinear response to 2013; Jones et al. 2014). Hence, further studies should also
pCO2 increase as it has been observed with the temperate include scenarios with reduce POM load to better understand
shallow and symbiotic coral Oculina arbuscula, whose the importance of the nutritional status on the CWC response
calcification rate only decreased at a pCO2 above 2800 μatm to stress.
(Ries et al. 2010). Concerning L. pertusa, its calcification
declined by 26–29% during a short-term exposure (1 week)
to a 0.1 unit decrease in pH, but was slightly enhanced when 35.4 Respiration Rates
the corals were exposed to low pH for more than 6 months
(Form and Riebesell 2012). A lack of calcification decline at In aerobic organisms, such as CWC, the oxygen consumption
high pCO2 was also observed for L. pertusa and M. oculata rate or respiration is directly proportional to the basic
reared between 6 and 9 months at pH values expected by the metabolic rate, which corresponds to the rate of energy used
end of the century (Maier et al. 2013a; Movilla et al. 2014a), by an organism to support basic body functions essential for
and for D. cornigera after 11 months of culture (Movilla its maintenance (mainly the metabolic costs of protein
et al. 2014b). These studies therefore suggest that short-term turnover and ion homeostasis). Cellular respiration is thus a
experiments may underestimate the acclimation capacities of set of metabolic reactions that convert biochemical energy
CWC to OA and their capacity to maintain maximal from stored nutrients (sugars, fatty acids and amino acids)
calcification rates under carbonate chemistry changes. into adenosine triphosphate (ATP) required for metabolism.
Food availability can also influence CWC response to pH Respiration rates of many Mediterranean CWC species
decline. Until now, OA studies were performed with starved measured at their in situ temperatures are in the same order
corals (Maier et al. 2012), or corals fed with artificial food of magnitude, suggesting that these corals have the same
(Hennige et al. 2013; Carreiro-Silva et al. 2014; Movilla metabolic needs: Dendrophyllia cornigera (2.0 ± 0.3 μmol C
et al. 2014a,b; Rodolfo-Metalpa et al. 2015). Sometimes cm−2 day−1, Gori et al. 2014a), Lophelia. pertusa, Madrepora
artificial diet was used several years before the beginning of oculata (3.8 ± 1.0 and 3.2 ± 0.6 μmol C cm−2 day−1; Naumann
the experiment (e.g. Movilla et al. 2014a, b), inducing a coral et al. 2014), and Desmophyllum dianthus (3.0 ± 0.8 μmol C
metabolism probably completely different than the one they cm−2 day−1 in Naumann et al. 2011; 1.34 μmol C cm−2 and
display under natural conditions. Only one study (Rodolfo- 3.6 μmol C cm−2 in Gori et al. 2014b, 2016, respectively).
Metalpa et al. 2015) carried out a transplantation experiment Mediterranean CWC respiration rates are however lower
in the pCO2 vent of Ischia (Italy), with the aim to investigate than those measured in tropical corals (e.g. Stylophora
both natural OA and feeding conditions. Under both high pistillata maintained in the dark: 4.0–7.4 μmol C cm−2 day−1;
and low pCO2 conditions, calcification rates were 44% lower Houlbrèque et al. 2003), indicating a reduced metabolic
than those measured in aquaria with artificially fed corals (at activity in CWC compared to their warm water congeners.
similar temperature and pH). This experiment suggests that On the contrary, Atlantic L. pertusa respiration rates are
artificial feeding significantly changes the calcification rates lower than those measured from Mediterranean: 30% lower
and response of CWC to stress; however, CWC in Ischia for specimens of Scottish waters (Dodds et al. 2007) and
were transplanted in very shallow waters which are not the even lower for L. pertusa in the Norwegian fjords 75%
normal living area of CWC, which might have significantly (Larsson et al. 2013). Coral metabolic activity is indeed
differed in nutritional quality compared to the deep generally positively correlated to temperature (e.g. Edmunds
2005; Dodds et al. 2007; Naumann et al. 2014), independently Tisler Reef (Norway). The authors found that GoM
of the corals’ symbiotic state (Jacques and Pilson 1980). populations exhibited decrease in respiration rates,
Several other environmental factors affect CWC conversely the populations from the Tisler Reef displayed
respiration rates, such as zooplankton consumption. As higher respiration rates. These differences are likely the
zooplankton is a main source of nutrients rapidly convertible result of environmental disparities between the two regions,
into energy, respiration rates were positively correlated with invoking the potential for local adaptation or acclimatisation
grazing rates (Jacques and Pilson 1980; Naumann et al. to global change. The lack of understanding of how
2011; Gori et al. 2014b). In turn, zooplankton exclusion (i.e. biogeographically disconnected populations will answer to
starvation) reduced respiration rates of D. dianthus from the OA hampers our prediction capability.
Mediterranean by 20% after 1 week of maintenance in such
conditions, by 49% and 62% after 2 and 3 weeks respectively
(Naumann et al. 2011), and 39% after 28 weeks in L. pertusa 35.5 Organic Matter Fluxes
from Northeast Atlantic waters (Larsson et al. 2013).
Respiration rates were also observed to increase in parallel to It is well known from the first studies performed on tropical
seawater temperature, in L. pertusa sampled in Scotland corals that all coral species, including CWC, release organic
(from 9 to 11 °C, Dodds et al. 2007), D. cornigera from matter (OM) into the surrounding seawater, in dissolved
Spain (from 12 to 16 °C, Gori et al. 2014a; Reynaud (DOM) or particulate (POM) forms (Ferrier-Pagès et al.
unpublished data), in D. dianthus from Italy (Gori et al. 1998; Wild et al. 2008; Naumann et al. 2010), including
2016) and in Dendrophyllia ramea from Cyprus (from 20 to spawning products and mucus (e.g. Harrison et al. 1984;
24 °C Reynaud et al. unpublished data), suggesting that Crossland 1987; Brown and Bythell 2005; Bythell and Wild
corals can tightly control their metabolic activity within their 2011). Mucus is used to capture small food particles (Lewis
natural thermal range. Outside this thermal range, stress and Price 1975; Shimeta and Koehl 1997; Riisgard and
induced an abnormal elevation in CWC respiration rates Larsen 2010) and it is also considered as a protection against
(Khripounoff et al. 2014). Similarly, a 3–4 °C decrease in sedimentation (Schuhmacher 1977) and microbe infection
seawater temperature induced a parallel decline in respiration (Ritchie 2006; Bythell and Wild 2011). OM release makes an
rates of M. oculata (from 12 to 9 °C, Naumann et al. 2014) essential contribution to the ecological functioning of coral
and D. cornigera (from 12 to 8 °C, Gori et al. 2014a). This reefs, because it is degraded by prokaryotes through their
pattern was however not observed for all temperatures and extracellular enzyme activity and is used for bacterial growth
coral species: respiration rates were thus unaffected in L. (Cunha et al. 2010), or it enters into the recycling pathways
pertusa between 12 and 6 °C, nor in M. oculata between 9 of carbon and nitrogen (Wild et al. 2004). OM therefore
and 6 °C (Naumann et al. 2014), suggesting a wide thermal supports pelagic and benthic production and plays a major
tolerance window (perhaps due to regional differences and role in the nutrient cycles and trophic structure of reef
biogeographic variability) and/or strong physiological ecosystems (Bythell and Wild 2011). Recently, the impor-
capacity for thermal adjustment for these species to low tance of coral mucus to fuel the entire ecosystem via a sponge
temperatures. Laboratory experiments also showed that loop has also been demonstrated in tropical reefs (Rix et al.
respiration rates were unaffected by acidification in many 2016). Both healthy and stressed corals can take up particu-
CWC species (Maier et al. 2013b, 2016; Rodolfo-Metalpa late (Anthony 1999, 2000; Ferrier-Pagès et al. 2011) and dis-
et al. 2015). It would have been expected that the up-regulation solved OM (Tremblay et al. 2012; Levas et al. 2015) for their
of the internal pH under acidification stress would have own energetic needs. This is particularly important in deep-
required more energy, and thus higher respiration rates. This sea environments, which are considered to be energy-limited
discrepancy might be due to the corals feeding in laboratory ecosystems (McClain et al. 2012) and where CWCs have an
experiments, masking the real effect of acidification on the opportunistic feeding (Duineveld et al. 2007; van Oevelen
respiration rates (Carreiro-Silva et al. 2014; Rodolfo-Metalpa et al. 2009; Mueller et al. 2014). OM fluxes are therefore in
et al. 2015; Gori et al. 2016; Maier et al. 2016). Future two directions: from the corals to seawater and inversely. In
research should therefore aim to further investigate the effect general, POC release by the CWC tended to be lower, and
of short- and long-term starvation on the respiration rates of DOC release rates tended to be higher than rates reported for
CWC and combine both, starvation and environmental warm water corals. In CWC reefs, where more planktonic
stresses, to assess the resistance and resilience of food is usually available for the corals (Freiwald et al. 2004),
CWC. Another explanation for this discrepancy might be it may be energetically more favorable to release DOC into
partially due to natural variation among the studied the surrounding water.
populations (Georgian et al. 2016). These authors have tested Studies on OM fluxes have mainly been performed in
the physiological response of L. pertusa populations to three laboratory experiments, by measuring, over few hours, the
pH treatments in the Gulf of Mexico (GoM, USA) and the quality and quantity of OM released or taken up by a coral
Fig. 35.2 Incubation of

Dendrophyllia cornigera (a)
and Dendrophyllia ramea (b)
in closed chambers containing
a small magnet in order to
keep the water in movement
thanks to the magnetic plate
where the chambers are
placed. During the
incubations, rates of
calcification, respiration and
Total Organic Carbon (TOC)
excretion were measured.
Incubations last for 6 h.
(Photographs: © S. Reynaud)
colony reared in incubation chambers (Fig. 35.2). Several OM production can be species specific, as found for tropical
studies reported high amounts of total organic carbon (TOC), zooxanthellate corals (Naumann et al. 2010), or linked to the
or DOC, excreted by CWCs under their normal growth coral morphology (Lewis and Price 1975; Shimeta and Koehl
conditions and without a stimulus (Wild et al. 2008, 2010; 1997), since species with large polyps (D. cornigera and D.
Maier et al. 2011, 2016; Naumann et al. 2011, 2014; Gori dianthus), that can capture big preys, do not usually need to
et al. 2014a). Higher OM release rates were observed in release large amounts of mucus for small prey capture. The
response to food supply, mechanical and electrical huge discrepancy in OM production can also be due to the
disturbances (Shelton 1980; Mortensen et al. 2001; Zetsche differences in food quantity, quality and richness, the
et al. 2016), microorganisms’ infection and exposure to high seasonality in OM production, or related to the dynamic
concentrations of suspended sediment (Brooke et al. 2009; physical environment in which CWC reefs occur (Duineveld
Larsson et al. 2013). Depending on the type of stimuli, the et al. 2007; Davies et al. 2009; Purser et al. 2010; Findlay
quality of the released mucus can however be different (more et al. 2013).
or less “watery”), and will thus require more or less energetic Several environmental factors can affect OM fluxes in
investment (Zetsche et al. 2016). The use of digital CWCs, as already described above. However, temperature
holographic microscopy (DHM) also showed that mucus and feeding are the two main parameters tested on mucus
production starts from the thecal regions and moves from the release. A short-term (5 weeks) increase in temperature
calyx to the base of the coral polyp (Zetsche et al. 2016). The reduced TOC release rates in D. ramea, or D. cornigera
highest release rates for CWCs under natural conditions (unpublished data), while a long-term temperature increase
were observed for Lophelia pertusa from NE Atlantic (5 months) had no effect on the OM production by D.
(~9.6 μmol C cm−2 day−1, Wild et al. 2008, and 4.6 μmol C cornigera (Gori et al. 2014a). On the contrary, a temperature
cm−2 day−1, Maier et al. 2011) and Madrepora oculata decrease induced a shift from TOC release to uptake in D.
(4.2 μmol C cm−2 day−1, Maier et al. 2011). Lower release cornigera (Gori et al. 2014a). This finding is in agreement
rates were measured in Mediterranean corals, for with the significant reduction observed in coral metabolism
Dendrophyllia cornigera (0.88 ± 0.34 μmol C cm−2 day−1; at this low temperature, since OM release depends on the
Gori et al. 2014a) and Desmophyllum dianthus (0.4 μmol C corals’ metabolic activity (Wild et al. 2008; Naumann et al.
cm−2 day−1, Naumann et al. 2011). This large difference in 2011). Such a reduction was previously observed in tropical
corals when seawater temperature fell below their natural 2000), or induced by animal/human activities. Under
thermal range (Coles and Fadlallah 1991; Kemp et al. 2011). favorable conditions, these fragments can attach to a substrate
OM fluxes are also affected by the corals’ feeding status, but and develop into new colonies. Sexual reproduction (fusion
due to the high variability from one species to another one, of sperm and eggs) is however essential to maintain genetic
or even from one colony to another (e.g. in Maier et al. 2016, diversity of a species.
from −4.16 to 55.46 μmol TOC g−1 skeleton h−1), it’s difficult Little is known of the basic reproductive biology of CWC
to understand the effect of feeding and/or starvation on TOC and most observations were performed on few coral species,
release rates. Well-fed colonies of D. dianthus were shown to such as Lophelia pertusa (e.g. Waller and Tyler 2005; Brooke
release, mainly in the form of DOC, 7% of the daily organic and Järnegren 2013; Pires et al. 2014), Madrepora oculata
carbon uptake through zooplankton feeding (Wild et al. (Waller and Tyler 2005; Pires et al. 2014), Oculina varicosa
2008). Subsequent studies performed on Madrepora tended (Brooke and Young 2003), Enallopsammia rostrata,
to show however that TOC release rates were generally Solenosmilia variabilis (Burgess and Babcock 2005; Waller
higher for slightly fed or starved corals than for well-fed 2005; Pires et al. 2014), Goniocorella dumosa (Waller 2005)
corals (Maier et al. 2016; Baussant et al. 2017) (respectively and Fungiacyathus marenzelleri (Waller and Feehan 2013).
1.89 and −0.12 μmol g−1 skeleton h−1 for starved and fed In contrast to structure-forming colonial species, which
corals, Maier et al. 2016). appear to be uniformly gonochoristic broadcast spawners
The above studies clearly show that more investigations (Brooke and Young 2003; Burgess and Babcock 2005; Waller
are needed to fully understand which factors induce OM 2005; Waller and Tyler 2005; Pires et al. 2014), cold-water
release and/or uptake in CWC. Climate change can directly solitary scleractinians, such as Flabellum sp. (Waller et al.
or indirectly alter the quality and quantity of the released 2008; Mercier et al. 2011; Waller and Tyler 2011),
OM and change the associated bacterial diversity, as observed Caryophyllia sp. (Waller et al. 2005), and Fungiacyathus sp.
in tropical corals (Ainsworth and Hoegh-Guldberg 2009) (Waller et al. 2002; Flint et al. 2007; Waller and Feehan
and in CWC (see Weinbauer et al., this volume), likely 2013), have various reproductive features and strategies,
affecting OM degradation rates. Understanding how the including hermaphroditism, gonochorism, brooding, and
different stresses alter OM fluxes, microbial degradation broadcast spawning. It is impossible to distinguish the sex of
rates and microbial growth will improve our understanding individual polyps from external morphology. Gametes can
on future changes of the deep reef biogeochemical cycling, only be observed after fixation and decalcification (Brooke
remineralisation pathway and trophic structure. 2002; Waller 2003). Microscopic observations showed that
sperm develop in cysts held together by a mesogleal envelope
(spermacysts or spermatic cysts), while oocytes are often
35.6 Reproduction found in groups or ʻpocketsʼ, but without connection between
them. All gonads develop in the lamellae of the mesenteries,
Knowledge about reproductive seasonality, gamete quality, eventually migrating into the mesoglea (Brooke 2002; Waller
fecundity and larval supply is essential for understanding et al. 2002; Waller 2005; Waller and Feehan 2013).
ecosystem resilience and biogeographic dispersion. In Gametogenesis can be quasi-continuous in Caryophyllia
addition, the distribution pattern of larvae gives insights into species (Waller et al. 2002), in E. rostrata (Burgess and
population connectivity and colonisation of different oceanic Babcock 2005), or in F. marenzelleri (Waller et al. 2002,
areas. Reproduction is highly stress dependent (a coral will 2005; Waller and Feehan 2013) or clearly continuous in M.
stop reproducing when stressed) so the reproductive status of oculata (Pires et al. 2014). Gametogenesis can also be
coral populations can be used as a health proxy. For example, periodic, or seasonally-controlled in L. pertusa (Waller and
Waller and Tyler (2005) observed that under trawling stress Tyler 2005; Brooke and Järnegren 2013; Pires et al. 2014).
no Lophelia were sexually mature, while they were all in a The seasonal control is not through temperature or light
reproductive state in a preserved area. To survive to their (moon light) as in shallow species (Fadlallah 1983; Harrison
environment, corals have developed several asexual and Wallace 1990; Richmond and Hunter 1990), because
reproductive strategies: fragmentation (Highsmith 1982), CWC live in the dark and below the thermocline; therefore,
polyp bail-out (Rosen and Taylor 1969; Sammarco 1982), seasonal fluctuations in phytodetritus input from surface
parthenogenesis (Stoddart 1983; Ayre and Resing 1986; waters (Billett et al. 1983; Tyler et al. 1992, 1993; Rice and
Yeoh and Dai 2010), or production of genetically identical Lambshead 1994) may rather control reproduction (Waller
larvae due to cleavage (Heyward and Negri 2012). To date, and Tyler 2005; Mercier et al. 2011; Brooke and Järnegren
fragmentation is the only known mode of asexual 2013). However, this is not the case for L. pertusa, as well as
reproduction in L. pertusa (Dahl et al. 2012). Fragmentation O. varicosa, since they produce a single cohort per year
occurs naturally when coral pieces are broken off a colony as (Brooke and Young 2003; Waller and Tyler 2005; Brooke and
a result of waves and storms for shallow corals (Lirman Järnegren 2013) of small oocytes (an average of 3300 oocytes
per cm2, 140 μm diameter maximum) and do not seem to be fertilisation. Such behavior avoids the risk of being eaten by
affected by food supply (Larsson et al. 2014). benthic predators (Brooke and Young 2003), and/or is a way
Most CWC species, such as the reef builders L. pertusa to reach the photic layer with a higher quality and quantity of
and M. oculata are gonochoric, i.e. males and females exist food.
as separate individuals (Brooke and Young 2003; Burgess It is obvious from the few observations above that more
and Babcock 2005; Waller 2005; Kerr et al. 2010; Pires et al. work is needed on CWC reproduction and especially on the
2014), while their tropical congeners are rather larval stages, which are particularly understudied. For
hermaphroditic, i.e. the same polyp displays both active male instance, future experiments assessing the impact of low pH
and female gonads (Fadlallah 1983; Richmond and Hunter on the reproductive investment would be crucial for
1990; Harrison 2011). Only the genus Caryophyllia (Waller understanding the response of CWC to OA.
et al. 2005), and Flabellum (Mercier et al. 2011; Waller and
Tyler 2011) are hermaphroditic CWC. Gonochorism is a
more primitive adaptation than hermaphroditism (Goffredo 35.7 Conclusions
et al. 2002) and may be more important for maintaining
genetic diversity (Szmant 1986). In addition, all CWC Although CWCs function as ecosystem engineers in many
investigated to date are broadcast spawners, releasing sperm deep environments, they have received significantly less
or eggs near-continually in the water column and preventing attention than shallow tropical and temperate corals, whose
self-fertilisation (Waller 2005; Waller and Feehan 2013; physiology and holobiont composition have been extensively
Pires et al. 2014), while some tropical, and Antarctic sea studied. CWC are, however, severely affected by
anemona species (Rodriguez et al. 2013) can also be brooders anthropogenic changes or pollution, and therefore deserve
(internal fertilisation and embryogenesis before releasing further research, particularly at the physiological level, for
larvae). processes such as calcification, growth, reproduction or
The larval stage has been poorly studied in CWC, due to feeding. Such knowledge is required to understand which
the difficulty in observing larvae at several hundreds or environmental factors determine the abundance and
thousands of meters depth. Like many species of shallow- development of CWC in the Mediterranean Sea, as well as
water reef corals, deep-sea species need hard substrates for their response to climate-change induced perturbations.
larval settlement. Deep-water coral species therefore settle More basic research on the CWC trophic ecology is needed
on dead scleractinian skeletons, rock fragments, shells or to assess which type of food is available in deep waters and
Polychaeta tubes (Rogers 1999). The larval lifespan has only understand how resource supply and demand by CWC
been studied under laboratory conditions. A larval lifespan determine their relative abundance in the deep oceans.
of 14–21 days has been observed for the coral O. varicosa, Overall, understanding deep food webs will help to more
before settlement on a hard substratum (Brooke 2002; accurately assess the function of these complex reef systems
Brooke and Young 2003), while a lifespan of 8 weeks was and predict how they will be affected by climate change. In
recorded for the larvae of L. pertusa (Larsson et al. 2014). In addition, targeting knowledge gaps in CWC life history
addition, Rinkevich and Loya (1979) first stipulated that all (such as growth rates, age, size of reproductive maturity,
CWC larvae are lecithotrophic, i.e. they feed only after larval dispersal, etc.…) will be essential for conservation and
settlement and metamorphosis. This is in agreement with the management of CWC species worldwide.
observations of large mature oocytes in M. oculata, S.
variabilis and E. rostrata. However, Larsson et al. (2014) Acknowledgements The authors wish to acknowledge the
observed that L. pertusa larvae were rather planktotrophic as CYCLAMEN project funded by the TOTAL foundation (BIO_
2014_091_Juin_CS-8). The authors are thankful for the comments
previously suggested by Waller and Tyler (2005). Before made by the reviewers that contributed to improve this paper.
settlement, larvae have thus a planktonic life, and their
swimming behavior is similar to that of other scleractinian
larvae. Most larvae swim in a rotary clockwise or counter-
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Growth Patterns of Mediterranean
Calcifying Cold-Water Corals 36
Franck Lartaud, Vincent Mouchi, Leïla Chapron,
Anne-Leïla Meistertzheim, and Nadine Le Bris
Abstract current understanding of scleractinian cold-water coral

Skeletal growth is a key physiological function, which in growth patterns. The main environmental parameters
the case of calcifying organisms, provides support for that control calcification and their influence on cold-
the general colony structure together, whilst simultane- water corals in the context of ongoing global environ-
ously providing protection for internal soft tissues. mental change are illustrated with examples from studies
Given this fundamental importance, growth patterns can conducted with different calcifying species from the
therefore reflect the health status of organisms. Mediterranean Sea, utilising both aquaria and in situ
Additionally, engineer species forming 3D structures, experimental studies.
such as scleractinian cold-water corals, enhance local
biodiversity through the provision of new structural and Keywords
hydrodynamic habitats. Furthermore, cold-water corals Scleractinia · Skeleton · Calcification · Environmental
may be used as paleoclimate indicators, and act as factors · Forecast of reef growth · Cold-water corals ·
sources for novel pharmaceutical compounds as well as Mediterranean
represent significant sinks for CO2 sequestration. At
time of writing, cold-water coral reefs are facing several
serious threats, particularly in the Mediterranean Sea,
where the combined effects of climate change and other 36.1 Introduction
anthropogenic environmental disturbances are interact-
ing in regions of coral colonisation. The characterisation The appearance of hard structure calcifying fauna during
of the Mediterranean cold-water coral growth patterns is the Cambrian was a major step in the evolution of the ani-
thus a crucial step for accurate forecasting of reef resil- mal kingdom tightly linked with the global CO32− and CO2
ience under environmental change and for the establish- budgets. The skeleton secreted by these fauna both sup-
ment of adequate conservation strategies. From the ports the general shape of the organism as well as protects
organisation of soft tissues to the resulting mineralogical soft tissues against biotic (e.g., predation) or abiotic
structures formed from the polyp to the reef scale, this threats. Though a range of substances may be secreted to
chapter gives an overview of the state of the art of the form hard structure skeletons, calcium carbonate based
skeletal structure are the most abundant and diversified in
terms of mineralogy and structure. Shells and skeletons
F. Lartaud (*) · L. Chapron · N. Le Bris
Sorbonne Université, CNRS, Laboratoire d’Ecogéochimie des may be made from a range of calcium carbonate com-
Environnements Benthiques, LECOB, pounds (e.g. aragonite, low or high-magnesium calcite,
Observatoire Océanologique, F-66650 Banyuls-sur-mer, France amorphous calcium carbonate), and dozens of microstruc-
e-mail: [email protected] tures have been identified among which the most wide-
V. Mouchi spread are prismatic, fibro-prismatic, nacreous and
Sorbonne Université, CNRS, Institut des Sciences de la Terre de crossed-lamellar (Carter 1980).
Paris (ISTep), F-75005 Paris, France
Calcifying species build their skeletons by the periodic
A.-L. Meistertzheim addition of carbonate. Both environmental conditions and
Sorbonne Université, CNRS, Laboratoire d’Océanographie
Mirobienne, LOMIC, Observatoire Océanologique, metabolic activity control the rhythm and growth rates of
F-66650 Banyuls-sur-mer, France the biomineralising fauna and deposition rate of the carbon-

https://doi.org/10.1007/978-3-319-91608-8_36
406 F. Lartaud et al.
ate material. Together with respiration, reproduction and 36.2 Living Tissues and Calcified Material
energy storage, calcification is one of the key physiological
indicators of organism fitness in calcifying fauna. 36.2.1 Anatomy of Corals
Biomineralisation studies offer the capacity to address
research questions on both short-term (i.e., hourly to daily) Corals are characterised by stinging cells (cnidocytes) that
and long-term (i.e., annual or multi-annual) scales, with a are used for prey capture and as a defence mechanism against
dual perspective: (1) to address the rapid response of organ- predators. Each polyp is made of two cell layers: ectodermal
isms to biotic and/or abiotic changes in the ecosystem, and and endodermal layers, separated by the mesoglea which is a
(2) to assess the resilience of calcifying species to ongoing collagen network (Allemand et al. 2004). The polyps are
and persistant environmental change. Additionally, calcify- linked together by the coenosarc made by an oral (facing sea-
ing organisms may be used as oceanographic and water) and aboral (facing skeleton) epithelium. Polyps and
paleoceanographic environmental archives, by the analysis coenosarc thus cover the skeleton much like a glove
of geochemical proxies locked within their carbonate skel- (Fig. 36.1), leading to an endogenous biomineralisation.
etons at the time of deposition. In particular, changes in Biomineralisation occurs in a submicrometric interface
deep-water mass dynamics can be inferred from trace metal between the cells and the skeleton known as the extracellular
and isotope analyses of cold-water coral (CWC) skeletons calcifying medium, from an organic matrix composed of a
(Montero-Serrano et al. 2013). mixture of proteins, glycoproteins, and polysaccharides that
As it is the case for their shallow water counterparts, precisely self-assemble and control the CaCO3 crystal forma-
CWCs act as ecosystem engineers, forming reefs in cold tion (Allemand et al. 2011). Different functions have been
and deep waters. Indeed, scleractinian corals form three- attributed to this organic matrix, including control of the con-
dimensional structures, potentially accumulating over mil- centration of precursor ions, constitution of a tridimensional
lennia following death, that provide various ecological framework, template for crystal nucleation, for determination
niches for associated fauna, including feeding, spawning of the calcium carbonate polymorph, control of crystal elon-
and nursery habitats for a variety of species (Rueda et al., gation, inhibition of crystal growth, determination of spatial
this volume; D’Onghia, this volume). As a result, corals are arrangement of crystal units, and involvement with enzymatic
key species that partially support the biodiversity of marine functions and cell signalling (Marin et al. 2008).
ecosystems. Hence, reef-building scleractinian corals are During the calcification process, carbonic anhydrase is
species of great ecological value. In the Mediterranean Sea involved in hydration/dehydration reactions by supplying dis-
there are several locations where well developed CWC eco- solved inorganic carbon to the calcification site and removing
systems have been described, such as the Santa Maria di carbonic acid from the calcification site. This process is per-
Leuca coral province in the Ionian Sea (Vertino et al. 2010; formed by the metabolic conversion of CO2 into HCO3− and
D’Onghia et al. 2011; Chimienti et al., this volume) and the HCO3− into CO32− (Bertucci et al. 2013). Finally, the nucle-
submarine canyons of the Gulf of Lion (Orejas et al. 2009; ation – the pathfinder for crystal formation in the extracellular
Fiala-Medioni et al. 2012; Gori et al. 2013; Fourt et al., this calcifying medium – allows the formation of an initial ther-
volume; Puig and Gili, this volume) and Catalan Margin modynamically unstable mineral form, the amorphous cal-
(Lastras et al. 2016, this volume; Aymà et al., this volume). cium carbonate, prior to its transformation into aragonite. As
The biology of CWCs is much less understood than that an example, for the shallow-water coral Stylophora pistillata
of tropical corals, but during the last few decades significant from the Gulf of Aqaba, this transient skeletal compartment
research efforts have been dedicated to the characterisation has a short half-life (12.9 min) compared to the bulk of the
of CWC physiology and ecology (Roberts et al. 2009). The skeleton (167 h) (Tambutté et al. 1996). The resulting struc-
analysis of CWC growth patterns to date has been based on ture is thus composed of self-assembled aragonite minerals
both aquaria and in situ studies. Many studies have been con- with an inter- and intracrystalline organic matrix.
ducted in the North-East Atlantic and in the Gulf of Mexico,
though in recent years a substantial number of works focus-
ing on CWCs within the world ocean have been published, 36.2.2 Anatomical Particularities
including the Mediterranean. Many CWC studies conducted of Scleractinian Cold-Water Corals
in the Mediterranean have been focused in the influence of and Their Implications for Skeletal
temperature and acidification in these communities, being Growth
thus particularly relevant to the forecasting of CWC reef
resilience to global change (see Maier et al., this volume; Although reef-building CWCs exhibit many similar growth
Movilla, this volume). traits to other calcifying cnidarians, they also form some
distinct patterns in morphology which have to be taken into
36 Growth Patterns of Mediterranean Calcifying Cold-Water Corals 407
Fig. 36.1 Anatomy of two cold-water coral species from the Gulf of images as from (a) to (d) but corresponding in this case to a Madrepora
Lion, northwestern Mediterranean Sea. (a) Lophelia pertusa fragment oculata nubbin; note that in M oculata the coenosarc only connects the
showing polyp distribution along the skeleton with open polyps dis- polyps. Ten tentacles, cal calix, c coenosarc, pol polyp, mf mesenterial
playing the tentacles, (b) Lophelia polyps retracted inside the calices, filaments. Scale is 5 mm in (a–c) and (e–g) and 1 mm in (d) and (h).
(c, d) Coral tissues after decalcification showing polyp junction by both (Photographs © A.L. Meistertzheim (CNRS) and F. Lartaud (Sorbonne
mesenterial filaments and the ceonosarc cover, (e–h) Same sequence of University))
account in growth studies (Lartaud et al. 2017a). This is connected by both the coenosarc and mesenterial filaments,
particularly true for colonial species that form tree-like
located within the calix. This provides different pathways for
structures, such as Lophelia pertusa (recently synonymised molecule transfer within the tissues. On the opposite, M.
to Desmophyllum pertusum) (Addamo et al. 2016), oculata grows with a clear separation between polyps, only
Madrepora oculata, Solenosmilia variabilis and connected by the thin coenosarc. This leads to a single route
Dendrophyllia cornigera. (i.e. the coenosarc) for molecule transfer inside the colony.
Even though CWC colonies display the same general Coral calcification also occurs extracellularly. This is par-
anatomy as many shallow-tropical corals, with polyps linked ticularly prevalent for azooxanthellate colonial corals such
externally together by the coenosarc tissues, CWCs tend to as L. pertusa, which produce large amounts of extracellular
exhibit larger polyps that extend linearly (Gass and Roberts mucus (EMS), which can contribute to the calcification of
2011; Lartaud et al. 2017a). A branch of colonial CWC is the parchment-like tube of the symbiotic worm Eunice nor-
formed by the successive addition of large calices, growing vegica (Roberts 2005) (Fig. 36.2). This mucus has various
directly on tip of previous generations of polyps, which can functions, such as acting as an antifouling agent, protecting
lead to a considerable separation between polyps (Fig. 36.1a, the coral skeleton from attacks from endolithic and boring
b, e, f), in contrast to the closely packed, tiny polyps often organisms, and also as an aid in removing sediment particles.
forming the colonial structure of most tropical corals The occurrence of identical protein patterns within EMS and
(Lartaud et al. 2017a). the newly formed aragonite suggests that EMS plays a cen-
The distance between polyps could also have conse- tral role in the calcification process of the skeletal parts
quences for energy distribution within a colony. (Reitner 2005). Mucus could also be involved in facilitating
Decalcification of coral skeletons shows that different spe- coral attachment to the substrate (e.g., rock, dead or still liv-
cies do not display the same patterns in soft tissue connec- ing corals), as it is frequently observed in situ, as well as in
tion (Fig. 36.1c, d, g, h). Lophelia pertusa polyps are association with corals maintained in aquaria (Fig. 36.3).
Fig. 36.2 Coral fragments where the calcification over the tube pro- pertusa polyps. (c) Calcified tube of E. norvegica by Madrepora ocu-
duced by the symbiotic worm Eunice norvegica can be seen. (a) E. lata. Those specimens were collected in the Lacaze-Duthiers canyon,
norvegica coming out from its tube (behind the oyster shell). (b) northwestern Mediterranean Sea. Scale bar is 1 cm. (Photographs ©
Opposite view of the same worm showing the tube covered by Lophelia F. Lartaud (Sorbonne University))
Fig. 36.3 (a) Coral extra-skeleton calcification at the base of Lophelia skeleton calcification, (d) Madrepora oculata colony from the Lacaze-
pertusa polyp when deployed lengthened in aquaria (highlighted by a Duthiers canyon covering a bivalve shell with extra-skeleton
red arrow). The specimen was collected in the Lacaze-Duthiers canyon, mineralisation (© UPMC-Fondation TOTAL). Scale bars are 5 mm.
northwestern Mediterranean Sea (b) lateral view of the polyp showing (Photographs © F. Lartaud (Sorbonne University))
the extra-polyp cementation, (c) view from the polyp basis of extra-
36.3 Skeleton Microstructure ters (Constantz 1989). The distribution of these structures
and Crystallography differs according to the species, with arrangements varying
from discrete clusters to continuous chains (Cohen and
36.3.1 Initiation of Calcification and Growth McConnaughey 2003). In Lophelia pertusa, they are organ-
Models ised in a continuous line from the base of the corallite up to
the calix, near the inner edge of the wall, as shown in the
The observation of scleractinian CWC skeletal features scanning electron microscope (SEM) image after treating the
reveals two types of microstructures. Aragonite fibres are the samples with an acid etching solution (Fig. 36.4a). These
main skeletal components, representing the vast majority of regions are located close to the starting point of diverting
the calcified volume. Spatially-restricted areas of micromet- fibres and are considered to be nucleation sites for calcifica-
ric scale are also present, traditionally called centers of calci- tion (Bryan and Hill 1941). Indeed, contrary to the meaning
fication (COC) and also referred to as early mineralisation of the traditional name (centers of calcification), these struc-
zones (EMZ) or rapid accretion deposits (RAD). These tures are not formed by a unique crystal (Fig. 36.4b), nor are
zones are characterised by granular crystals arranged in clus- they located at the physical middle of the coral wall. The
the later, COCs are called Centres of Rapid Accretion (CRA)

and they are arranged into a Rapid Accretion Front (RAF).
CRA and RAF form deposits composing of a mineral phase
as well as an organic phase (dCRA and dRAF, respectively),
themselves recovered by successive layers of mainly mineral
Thickening Deposits (TD).
In the calcifying space, the supersaturation state allows
spontaneous formation of nucleation clusters comprised of
hydrated ions (Cölfen and Antonietti 2005). As these clusters
grow, they eventually become critical crystal nuclei, puta-
tively composed of amorphous calcium carbonate (ACC),
which is thought to act as a precursor of mineralised calcium
carbonate (Addadi et al. 2003). ACC is known to be present
in numerous biominerals (Weiner et al. 2003), but its pres-
ence in coral skeletons is debated (Cuif and Dauphin 1998;
Falini et al. 2013). Proteins and polysaccharides present in
the matrix fix themselves around these nanoparticles and
induce a stabilisation of the particles that can orientate them-
selves for association with other similar nuclei. By forming
clusters and welding, they are able to form single crystals
(Cartwright et al. 2012).
After putative ACC turned into nanometric crystals, ara-
gonite fibres (located in the TD region) grow from these
RADs to form sclerodermites, shaped in fans towards the
external side of the skeleton and polyp to increase skeleton
thickness.
Fig. 36.4 (a) Microstructures in the wall of Lophelia pertusa skeleton
from the Whittard canyon (NE Atlantic) under SEM, showing the Rapid
Accretion Deposit (RAD) arranged in a continuous line and the
Thickening Deposits (TD) layers made of aragonite fibres. Longitudinal 36.3.2 Growth Structures in the Thickening
growth direction is from left to right. Scale bar: 200 μm. ext. external Deposits Region
part of the skeleton, int. internal part, located in the calix, (b) Detail of
the bottom left part of (a) included in the red rectangle. SEM view of
layers in aragonite fibres near the RAD on the internal edge of the skel- The skeleton resulting from sclerodermite formation is not
eton. Scale bar: 10 μm homogenous. Density layers, such as the annual bands
formed in tropical corals have not been observed in CWCs,
COCs (or RADs) are the first biomineralised structures to but growth structures defined by opaque and translucent
appear in the wall formation (Rollion-Bard and Blamart bands in the coral wall have been seen under transmitted
2014), and this term is generally used in regards to their ini- light of L. pertusa from Sweden (Wainwright 1964) and
tial support role in further crystallisation events. Desmophyllum dianthus collected from the NW Atlantic
Since the granular crystals have a sub-micron size, it is (Lazier et al. 1999). These optically visible bands were origi-
likely that part of the calcification process is intracellular nally interpreted as annual patterns (Risk et al. 2005). The
(Constantz 1989). Vesicles have been observed in the apical bands were thought to have been formed by successive
membrane of the epithelium which are probably responsible nucleation phases during the life of the polyp, associated
for providing some material to the calcifying space (Johnston with advances and retreats of the outer tissue layer that cov-
1980), as they can be a pathway for seawater. Though no ers the corallite (Lazier et al. 1999). It has been demonstrated
mineralised structures have been observed in these vesicles, that the opaque and translucent bands are indeed thickening
they may act as stabilisation sites for amorphous calcium phases of the wall but their temporal meaning is probably not
carbonate (Cohen and McConnaughey 2003; Rollion-Bard uniform. Indeed, Gass and Roberts (2011) found the same
et al. 2010). amount of annual banding in living polyps of different ages
It is widely agreed that the calicoblastic layer plays a role from the same L. pertusa colony growing on North Sea oil
in calcification (Tambutté et al. 2011); however different platforms. As a result of this analysis, it seems that these
models grant it a more or less important function in this pro- bands are not useful to establish temporal calibrations of
cess: a direct control of the calicoblastic layer (Barnes 1970; polyp age.
Johnston 1980), a two-steps model (Cuif and Dauphin 1998; Recently, new microlayers (20–100 μm width) were
Cuif et al. 2011), and a layered model (Stolarski 2003). In observed under SEM after light etching of skeletal sections
Fig. 36.5 (a) SEM view of

Thickening Deposits (TD) in
the middle of the wall of a
Lophelia pertusa specimen
from the Porcupine Seabight
(NE Atlantic), showing
different packets of aragonite
fibre orientations. Scale bar
100 μm, (b) interpretation of
the SEM image from (a):
Black lines represent
subhorizontal fibres, grey
lines represent oblique fibers
and circles represent
subvertical fibers compared to
the section. Longitudinal
growth is from left to right
and radial growth from top to
bottom
from L. pertusa of the NE Atlantic and the Mediterranean the theca and the septa of L. pertusa from Norway, but with-
Sea (Mouchi et al. 2014). General growth rates and stron- out clear temporal pattern. Thin microlayers (<10 μm) have
tium fluctuations across an orthogonal transect to these been observed in the septa of the cup coral D. dianthus
increments tend to indicate that each microlayer corresponds (Lazier et al. 1999) and the authors suggested a possible rela-
to a period of one lunar month of growth. Though temporal tionship between these microlayers and biological clocks,
calibration of the skeleton from these microlayers is promis- such as (real or inherited) feeding cycles. Still, further chron-
ing, it is often hampered by the apparent lateral discontinuity ological calibration is required to improve the understanding
of these structures, particularly when occurring in opaque of skeletal growth in time and space, and facilitate the inter-
bands. From SEM observations of L. pertusa specimens, pretations of analysed transects of geochemical proxies in
taken from a variety of locations in the NE Atlantic and the terms of climatic conditions, as was the case for tropical cor-
Mediterranean Sea, coral skeletons seem to exhibit succes- als and the identification of annual banding.
sive growth phases in all three dimensions (Fig. 36.5) that
prevents continuity of microlayers (Mouchi et al. 2014).
It is also worthwhile mentioning that no bands or layers 36.4 S
ynthesis of the Different Methods
have been observed in L. pertusa by Mouchi et al. (2014) Used for CWC Growth Measurements
which may indicate growth patterns along the longitudinal
axis (i.e., in the maximum growth direction of the corallite). Contrary to solitary polyps such as Desmophyllum dianthus
Still, longitudinal growth do occur as indicated by proof of collected from the NW Atlantic, which form their skeleton
crystal growth competition on solely one side of scleroder- along a unidirectional growth axis, the structural complexity
mites (i.e., the side facing the basis of the corallite with pre- inferred by the three-dimensional morphology of colonial
existing sclerodermites), while the other side (opposite to the species (both stony and soft corals) makes it more difficult to
basis) is well ordered without disturbance (Mouchi et al. measure colony growth. Additionally, compared to their
2017). Mortensen and Rapp (1998) described white and dark shallow-water counterparts, direct measurements of growth
lines in both the transverse and the longitudinal sections of are constrained by the limited accessibility to deep-waters
where CWCs live. As a result, in situ growth studies are still logical or sclerochemical tools. Radiometric dating is also
scarce for CWCs compared to other biogenic carbonates. used to determine the rates of extension.
Methods to gauge the skeletal growth patterns of colo- The third group of methods investigates the renewal rate
nial CWCs are mainly derived from those developed for the of the colony, by determining the budding rate (i.e. new
investigation of shallow-water scleractinians. They include polyp addition over a period of time) (see Mortensen 2001;
both non-destructive methods and those which require the Lartaud et al. 2014). Due to logistical constraints and the
sacrifice of live coral fragments. Some methods can only be long life cycle of many CWC species, the modelling approach
used in aquaria experiments, whereas others can be imple- (Galli et al. 2016) is a further promising technique for the
mented under in situ conditions. All of these methods pro- study of CWC growth patterns.
vide useful complementary information but with several
restrictions. The selection of the method is determined by
the scientific objectives of the studies and the time avail- 36.4.1 Alkalinity Anomaly
able to conduct the study. In situ direct observations are
suitable for the study at colony level, but the specific role of Alkalinity anomaly is a commonly used technique to esti-
various parameters influencing growth can be difficult to mate skeletal growth. Measures take place in closed cham-
interpret. Regarding aquaria experiments, the complexity bers where coral fragments are incubated; water samples are
of the natural habitat is difficult to mimic, but the advantage collected from the chambers at the beginning and at the end
of this kind of experiments is that the environmental condi- of the experimental period. The water volume of the cham-
tions can be manipulated, with results of experimental stud- bers needs to be small enough to allow an accurate measure
ies therefore providing insight into the understanding of the of potential changes in the total alkalinity (AT). Calcification
potential drivers and environmental controls on CWC rates use the 2:1 stoichiometric relationship between the
growth (see Orejas et al., this volume). Whenever possible, decrease of AT and CaCO3 precipitation (Chisholm and
in situ experiments are recommended, in order to investi- Gattuso 1991). A correction must be applied for the changes
gate the influence of environmental variability and the of AT due to the significant release of inorganic nutrients dur-
combination of abiotic factors in their natural habitats on ing incubation, as has been documented for L. pertusa and
coral growth processes (e.g., Brooke and Young 2009 for M. oculata collected from the Lacaze-Duthiers canyon in the
Lophelia pertusa in the Gulf of Mexico and Lartaud et al. Gulf of Lion (Maier et al. 2013). The alkalinity anomaly
2014 for Mediterranean L. pertusa and Madrepora technique is however not always applicable for long-term
oculata). experiments due to several side-effects on the water chemis-
The main methods for the study of CWC growth can be try (e.g. microbial activity of biofilters, water exchanges,
summarised into different sets of techniques, each providing feeding) which are indistinguishable from the corals’ calcifi-
different types of information. cation activity (Form and Riebesell 2012 in L. pertusa from
The first group relates to techniques that measure calcifi- the Norwegian coast).
cation rates (generally expressed as g CaCO3 g−1 skeleton
day−1 or % day−1). These techniques are mainly used in
aquaria experiments to test the causal relationship between 36.4.2 Buoyant Weight
physicochemical changes in water chemistry and the
biomineralisation response of the CWCs (e.g., Orejas et al. The buoyant weight technique is a common method used for
2011a, b; Naumann et al. 2014; Gori et al. 2014; Rodolfo CWC growth experiments in aquaria. Calcification is inferred
Metalpa et al. 2015 for L. pertusa, M. oculata, Dendrophyllia from changes in weight of the living organism in seawater of
cornigera and D. dianthus from the Mediterranean Sea). known density. The method is based on the Archimedes’
The techniques most frequently used to measure calcifica- Principle and a correction factor is applied as it has been
tion rates are: the alkalinity anomaly, the buoyant weight or observed that tissue weight accounts for 3–4% of the skeletal
the radioisotope techniques (Maier et al. 2009; Form and buoyant weight for M. oculata from Cap de Creus canyon in
Riebesell 2012). the NW Mediterranean and L. pertusa from the Island of
The second group of techniques quantify linear or surface Malta (Orejas et al. 2011a) and 14 ± 4% for D. cornigera
growth rates (expressed in mm year−1 or cm2 year−1). These corals from Cap de Creus canyon and D. dianthus from the
methods can be used in aquaria and in situ (see Orejas et al. Island of Malta (Movilla et al. 2014b). The net buoyant
2011a; Lartaud et al. 2017b for L. pertusa, M. oculata, D. weight values of corals is converted into dry weight (DW)
cornigera and D. dianthus, in both cases with specimens using the density of the pure aragonite (2.94 g.cm−3) (Rodolfo
from the Mediterranean Sea). The surface and linear growth Metalpa et al. 2015 on D. dianthus from Malta and D. corni-
extension of coral fragments can be measured at the colony gera from the Ionian Sea). Although a negative influence of
level, or more accurately at polyp level using sclerochrono- handling cannot be excluded, this method is suitable for
measuring calcification over monthly intervals or longer and Sclerochronology is the “biomineral” equivalent to den-
it can be recommended for long-term rather than short-term drochronology used on trees. The concept is based on the
experiments. Results however need to be taken with caution assumption that each growth increment has been formed by
as potential artefacts of coral response can be associated to the organism in successive equivalent time intervals what-
long-term aquaria studies. ever their thickness (Knutson et al. 1972). The production of
carbonate structures by calcifying species periodically decel-
erates and eventually ceases, although environmental condi-
36.4.3 Radioisotopes tions still remain favourable for skeletal growth. Growth
increments (also called growth bands or growth rings) are
The radioisotope method involves the incubation of a fresh formed according to different periodicities, from infra-daily
coral fragment in a seawater volume containing radioactive to annual rates. The observations are made on skeletal sec-
elements (45Ca or 14C). After an incubation period of several tions (radial or longitudinal, depending on the species) under
minutes to hours, the coral pieces are rinsed in filtered sea- optical microscopy, scanning electron microscopy or X-ray
water, the tissue removed, the skeleton dried and dissolved fluorescence. The method is currently used for deep-water
with a strong acid and the incorporated radioactivity mea- octocorals and antipatharians (e.g., Sherwood et al. 2005 on
sured using a scintillation counter (e.g. Hennige et al. Primnoa resedaeformis collected offshore Nova Scotia,
2014b for L. pertusa from the Mingulay Reef Complex, NE Canada) and for shallow-water stony corals (Le Tissier et al.
Atlantic). The radioisotope method is highly accurate for 1994 on Porites lutea from Indo-Pacific and Porites porites
measurements at short timescales (periods can be minutes), from Caribbean Sea), but it is still rarely applied to sclerac-
but this method requires sacrificing the organism for analy- tinian CWCs due to limited knowledge on the growth period-
ses and is restricted to small volumes (e.g., 50 mL Falcon icity increments formation (Lartaud et al. 2017a and
tubes). references in Sect. 36.3.2 of this chapter).
The use of chemical markers is very useful, as they allow
a “time 0” point to be marked within the coral (i.e. the date
36.4.4 Surface and Linear Growth Extension of dye use), and the growth of the coral after this point can
then be measured. The incorporation of fluorochromes into
This is a useful technique, both for in situ and aquaria mea- the skeleton produces an internal fluorescent mark and sub-
surements. The growth measures are performed by means of sequently the growth increment can be readily estimated.
image analysis of photographs taken at different periods. The Calcein (Hassenrück et al. 2013 for D. dianthus from
surface extension provides information on the colony size Patagonia; Lartaud et al. 2013 for L. pertusa and M. oculata
changes (in cm2) (see Larcom et al. 2014 on L. pertusa from from the Gulf of Lion) and alizarin red (Brooke and Young
the Gulf of Mexico), and the linear growth extension high- 2009 for L. pertusa from the Gulf of Mexico; Form and
lights the growth rate (in mm year−1) of coral branches along Riebesell 2012 for L. pertusa from Norwegian coast) are
the main growth axis (Orejas et al. 2008 for L. pertusa and classically used in mark and recapture experiments with
M. oculata from Cap de Creus canyon, northwestern CWCs. However, recent comparison between calcein and
Mediterranean Sea; Orejas et al. 2011a for M. oculata and L. alizarin red stainings have shown that calcein appears more
pertusa from the Cap de Creus canyon and L. pertusa and D. suitable than alizarin red, as the last has been shown to
dianthus from the Island of Malta; Lartaud et al. 2017b for L. strongly limit growth of NW Mediterranean L. pertusa and
pertusa and M. oculata from the Lacaze-Duthiers canyon, M. oculata by delaying coral recovery following the treat-
NW Mediterranean Sea). Key benefits of this method are the ment (Lartaud et al. 2017b).
“low cost” of the approach and that the technique is non- Geochemical proxies (e.g., stable isotopes, minor and
destructive and particularly suitable for aquaria studies. trace metals) can also be analysed along the growth profile to
determine growth patterns. Sclerochemistry methods were
developed for shallow-water species, particularly for sclerac-
36.4.5 Sclerochronology and Sclerochemistry tinian corals (Pätzold 1984). However, the use of the sclero-
chemistry is limited with CWCs due to important
The analysis of growth increments (sclerochronology) or metabolically-induced skeleton geochemical changes (so
fluctuations of geochemical signals throughout the growth called “vital effects”), leading to an uptake of isotopes and
(sclerochemistry) requires sacrificing the organisms under elements during the ion transfer between seawater and skel-
study. These analyses however provide an accurate measure eton (Adkins et al. (2003) for L. pertusa and D. dianthus
of growth rates in coral stem and branches and/or time allow- from the NW Atlantic; López-Correa et al. (2010) for L. per-
ing a better characterisation of the temporal dynamics in tusa from the Santa Maria di Leuca coral province in the
CWC growth. Ionian Sea; Marali et al. (2013) for D. dianthus from the
Azores; Raddatz et al. (2013) for L. pertusa from various ony masses over time (see more details in Lartaud et al.
locations from the European continental margin). 2017a). Those models appear particularly relevant for the
study of ecological properties and their impacts on coral
growth under changing environmental conditions, such as
36.4.6 Radiometric Dating illustrated by Galli et al. (2016) on Corallium rubrum, an
endemic species to the Mediterranean Sea.
Radiometric or radioactive dating compares the abundance
of a naturally occurring radioactive isotope within the skel-
eton to the abundance of its decay products, which form at a 36.5 Growth: From the Colony to the Reef
constant rate. Different techniques are used for CWC spe-
cies, including 14C (Roark et al. 2006 for Corallium secun- 36.5.1 Extension of the Colony
dum, Gerardia sp. and Leiopathes glaberrima off Hawaii),
230
Th-U (Cheng et al. 2000 for D. dianthus from the Pacific, For scleractinian corals, colony-growth rate measurements
Atlantic and Southern Oceans) and 210Pb-226Ra (Sabatier refer mainly to the linear extension (increase in length),
et al. 2012 for L. pertusa and M. oculata from Røst Reef, off whereas growth rate estimates for soft corals (gorgonian,
Norway). Initially applied for ageing fossil-reef structures, zoanthid and antipatharian species) mostly derive from radial
radiogenic isotopes are also useful to determine the life span thickening analysis. As they form the largest reef structures
of long-lived species when ring counting is not possible. across many regions of the North and South Atlantic, as well
as the Mediterranean, growth studies were principally dedi-
cated to Lophelia pertusa. In contrast, little effort has thus far
36.4.7 Budding Rate been dedicated at determining growth rates of other
Mediterranean scleractinians such as Madrepora oculata,
Colonial CWCs (such as L. pertusa and M. oculata) produce Dendrophyllia cornigera or Dianthus dianthus.
large polyps compared to octocorals and most tropical Lophelia pertusa exhibits the highest growth rates from
scleractinians. Colony growth is primarily driven by the
all CWC known species thus far investigated, ranging from
addition of new polyps (Gass and Roberts 2011). Quantifying 0.01 to 38.1 mm year−1 (see Table 36.1 and Roberts et al.
the new polyp additions over a period of time (budding rate) 2009). The reason for this large inter-individual variability
is a useful and non-destructive technique to measure colony- is unknown. At present, no clear influence of bathymetry
growth. Comparison between studies is however difficult as has been detected in CWC growth rates. However different
different works start with different polyp number. A stan- environmental conditions can contribute to partially explain
dardised method was proposed by Lartaud et al. (2014) for L. the high variability recorded in L. pertusa growth rates.
pertusa and M. oculata from the Lacaze-Duthiers canyon, Environmental variability can be considered at different
NW Mediterranean Sea, using the rate of new polyp addition scales (e.g. between oceans or at the habitat scale) and local
per polyp initially present per year (expressed in %). topography or current flow exposition may explain the
large growth fluctuations observed within the same geo-
graphic area. An example of these local variations are the
36.4.8 Growth Modelling growth rates recorded for corals from two different loca-
tions in the western Mediterranean: (1) 2.2–17 mm year−1,
A complementary approach to the direct measurement of for specimens collected at ~200 m in the Cap de Creus can-
growth is CWC modelling. Numerical simulation techniques yon (Orejas et al. 2008, 2011a) and (2) 0.01–38.1 mm
for marine fauna have been developed across different scales, year−1 for specimens growing at ~500 m in the Lacaze-
ranging from small-scale physiological processes to whole Duthiers canyon (Lartaud et al. 2014, 2017b). This example
ecosystem dynamics. Organism and population growth mod- also shows that Mediterranean CWC specimens of L. per-
els are based on the “bioenergetics approach”, calibrated tusa can reach similar maximum growth rates to those
with experimental observations. A bioenergetic growth observed to date in the North Sea and in the Gulf of Mexico
model describes growth as the evolution of a quantity (maximum observed of 34 mm year−1 in the North Sea
(energy, biomass or mass of a specific compound) over time (Gass and Roberts 2006) and 32.3 mm year−1 in the Gulf of
through the balance of input and output fluxes, through the Mexico (Larcom et al. 2014)). Finally, in situ tag and recap-
system boundary and between compartments within the sys- ture techniques have shown a decrease in colony growth
tem. The simplest formula considers one single compartment rate over time (Fig. 36.6). This may reflect faster growth in
for biomass (or energy), one input and one output flux that younger colonies (Larcom et al. 2014) and suggest that the
depend on the system biomass/energy usage according to age of a colony could also play an important role, partially
allometric laws (Glazier 2005). The resulting estimations explaining differences between growth rate measurements
typically allow forecasting of the number of polyps and col- (Table 36.1).
Table 36.1 Linear extension (in mm year−1) measured for scleractinian cold-water corals from different locations
Growth rates
Species Localisation Depth (m) (mm.year−1) Method References
Lophelia pertusa Central Mediterranean 300 15–17 Aquaria Orejas et al. (2008)
Sea
Lophelia pertusa Central Mediterranean 300 8.8 ± 6.6 Aquaria Orejas et al. (2011a)
Sea
Lophelia pertusa Western Mediterranean 520 1.3 ± 1.5 (old) – 7.5 ± In situ mark and recapture Lartaud et al. (2013)
Sea 1.2 (young polyps)
Lophelia pertusa Western Mediterranean 520 0.01–12.1 In situ deployment and Lartaud et al. (2014)
Sea recapture
Lophelia pertusa Western Mediterranean 480–520 2.2–38.1 In situ mark and recapture Lartaud et al. (2017b)
Sea
Lophelia pertusa Northeast Atlantic 955–1005 7.0 Observations of colonies from Duncan (1877)
man-made structure
Lophelia pertusa Northeast Atlantic 800 6.0 Observations of colonies from Wilson (1979)
man-made structure
Lophelia pertusa Northeast Atlantic 220 2.2–5.0 U-Th dating Pons-Branchu et al.
(2005)
Lophelia pertusa North Sea 60–110 26.0 Observations of colonies from Bell and Smith (1999)
man-made structure
Lophelia pertusa North Sea 100 5.0 Observations of colonies from Roberts (2002)
man-made structure
Lophelia pertusa North Sea 90–115 19.0–34.0 Observations of colonies from Gass and Roberts
man-made structure (2006)
Lophelia pertusa Norway 300 25.0 Sclerochemistry Mikkelsen et al. (1982)
Lophelia pertusa Norway 250 19.0 Sclerochemistry Freiwald et al. (1997)
Lophelia pertusa Norway 200–350 6.0 Sclerochemistry Mortensen and Rapp
(1998)
Lophelia pertusa Norway 80–315 9.4 Aquaria Mortensen (2001)
Lophelia pertusa Norway 340 8.0 Pb-Ra dating Sabatier et al. (2012)
Lophelia pertusa Gulf of Mexico 460–510 2.4–3.8 In situ mark and recapture Brooke and Young
(2009)
Lophelia pertusa Gulf of Mexico 200–800 3.2–32.3 Observations of colonies from Larcom et al. (2014)
man-made structure
Madrepora Western Mediterranean 250 3.0–18.0 Aquaria Orejas et al. (2008)
oculata Sea
Madrepora Western Mediterranean 250 5.1 ± 2.6 Aquaria Orejas et al. (2011a)
oculata Sea
Madrepora Western Mediterranean 520 1.2 ± 1.2 (old) – 3.5 ± In situ mark and recapture Lartaud et al. (2013)
oculata Sea 2.1 (young polyps)
Madrepora Western Mediterranean 520 0.5–8.4 In situ deployment and Lartaud et al. (2014)
oculata Sea recapture
Madrepora Western Mediterranean 480–520 0.01–18.0 In situ mark and recapture Lartaud et al. (2017b)
oculata Sea
Madrepora Norway 340 14.4 ± 1.1 Pb-Ra dating Sabatier et al. (2012)
oculata
Oculina varicosa Florida 80 16 Reed (2002)
Enallopsammia North Atlantic 1410 5.0 Pb-Ra dating Adkins et al. (2004)
rostrata
Solenosmilia Tasmania 890–1455 0.84–1.25 14
C dating Fallon et al. (2014)
variabilis
Desmophyllum Atlantic, Pacific, 420–2200 0.1–3.0 U-Th dating Cheng et al. (2000)
dianthus Southern Oceans
Desmophyllum 0.5–1.0 U-Th and 14C dating Risk et al. (2002)
dianthus
Desmophyllum South Pacific 0.5–2.0 Pb-Ra dating Adkins et al. (2004)
dianthus
(continued)
Growth rates
Species Localisation Depth (m) (mm.year−1) Method References
Desmophyllum Patagonia 25 2 Observations of colonies from Försterra and
dianthus man-made structure Häussermann (2003)
Desmophyllum Patagonia 15–20 0.4–1.0 In situ mark and recapture Hassenrück et al.
dianthus (2013)
Fig. 36.6 Estimated growth 20

rates of coral nubbins L. pertusa (LDC, northwestern Mediterranean Sea, in situ)
18
throughout the experimental M. oculata (LDC, northwestern Mediterranean Sea, in situ)
time (in years: yr). LDC 16
Growth rate (mm.yr–1)

Lacaze-Duthiers Canyon. 14
(Adapted from Lartaud et al.
2014, 2017b) 12
10
8
6
4
2
0
0 0.2 0.4 0.6 0.8 1 1.2 1.4 1.6 1.8 2
Time of experiment (yr)
Madrepora oculata from the NW Mediterranean Sea seasonal change in hydrodynamic conditions that occurs in
shows mean growth rates ranging from 0.01 to 18 mm year−1 the canyon heads of the Gulf of Lion (NW Mediterranean).
(Orejas et al. 2008, 2011a; Lartaud et al. 2013, 2014, 2017b). For instance, the observed increase in budding rate during
These values are within the same range as those measured in the winter/spring period may be promoted by organic parti-
the Norwegian Sea for this species and elsewhere for other cle supply induced by episodes of dense water shelf cascades
colonial species, except for Solenosmilia variabilis which and associated resuspension events (Canals et al. 2006;
has been observed to have very slow growth rates (~1 mm Heussner et al. 2006; Palanques et al. 2006). The response to
year−1; Table 35.1). As for L. pertusa, a decrease in colony environmental changes seems however species-specific as L.
growth rate over time for M. oculata is observed (Fig. 36.6). pertusa specimens living in the same habitat display the
Currently, no data exist for the rates of extension of D. same growth rates throughout the year (Lartaud et al. 2014).
cornigera in its habitat. However, several studies have been This behaviour suggests more plasticity in the energetic
conducted with this species in aquaria, using the buoyant requirement of this species, likely associated with different
weight technique. D. cornigera displays growth rates of feeding strategies (Kiriakoulakis et al. 2005) and bacterial-
7–30% per year (Orejas et al. 2011a; Gori et al. 2014), which host associations (Meistertzheim et al. 2016). This growth
are similar to the calcification rates of the long-life span D. pattern contrasts with the seasonal reproductive cycle
dianthus (>200 years, Risk et al. 2002), with calcification described for L. pertusa but not for M. oculata (Waller and
rates of 11–33% (Orejas et al. 2011a; Rodolfo Metalpa et al. Tyler 2005).
2015). This last species exhibits growth rates lower than Differences in growth patterns also occur at a long term
3 mm year−1 (Table 36.1). scale. L. pertusa from the NE Atlantic produces micro-layers
according to monthly lunar cycle (28 days) and the Sr/Ca
composition inside the micro-layers revealed an additional
36.5.2 Growth Dynamics cycle related to semi-lunar oscillations (14 days) (Mouchi
et al. 2014). Drivers of those growth rate changes seem to be
In addition to long-term changes, seasonal differences in related to the hydrological context, as in the studied region of
growth rates have been identified. In the Lacaze-Duthiers the N Atlantic, rapid downwelling of surface waters are
canyon differences have been observed over the year for M. caused by hydraulic control of tidal flow, associated with
oculata growth patterns (budding and polyp growth rates) advection onto deep bottom water reefs during peak tides,
(Lartaud et al. 2014); these differences may be owed to the which periodically increase the availability of organic parti-
cles for coral colonies (Davies et al. 2009). As deep as 900 m to sedimentation (Larsson et al. 2013 on L. pertusa from
water depth, tidal influence induces substantial temperature south Norway).
changes (1.5–2 °C) and input of organic matter in canyon
ecosystems (van Haren et al. 2014). The thickness of carbon-
ate micro-layers varies according to growth rate changes, 36.5.4 Reef Formation
showing two slow phases during each year: one in winter
months likely caused by a decrease in food availability, with After settlement of a coral larva, asexual formation of new
the second possibly correlated with the gametogenesis period polyps drives extension of the colony in three dimensions.
(Mouchi et al. 2014). Self-recognition of adjacent coral colonies, as well as skele-
Similar micro-layers have been detected but poorly tal fusion in areas with low levels of aragonite crystal organ-
revealed in Mediterranean L. pertusa (Mouchi et al. 2014). isation and strong molecular bonding, facilitate ecosystem
To date, no chronological calibration has been done and engineering, as described for L. pertusa from Norway
more investigations of these structures in an ecosystem free (Hennige et al. 2014a). Morevover, coral skeleton cementa-
of strong tidal control would be of great interest to better tion can also occur between different species, such as for L.
determine the role of environmental or endogenous rhythms pertusa and M. oculata from the NW Mediterranean
on the biomineralisation of scleractinians. (Fig. 36.7), inducing spatial complexity of the living area.
Polyp death rates at the base of colonies increase with the
colony lifespan, and hence the proportion of dead coral
36.5.3 Main Environmental Parameters framework increases, leading to zonation of the habitat
Governing CWC Growth (Buhl-Mortensen et al. 2010). Other organisms actively pro-
mote reef aggregation as well, such as the symbiotic worm
A large number of environmental factors (e.g. temperature, Eunice norvegica, which stimulates excessive calcification
salinity, nutrient concentration, currents) and/or biotic of Norwegian L. pertusa (Roberts 2005; Mueller et al. 2013).
factors (symbiosis, predation, competition) can affect coral Coral calcification over the tube produced by worms living
calcification (Miller 1995). The direct impact and relative within the coral branches strengthens the framework by
importance of these various parameters on CWC growth thickening and connecting coral branches (Fig. 36.2).
remains to be defined, and most probably they will be differ-
ent for the different species. Laboratory studies suggest that
an increase in food supply (considering quality and quan-
tity), rather than temperature, may be more important in
determining growth rates of scleractinian CWCs (as seen for
L. pertusa from Norway by Mortensen 2001 and M. oculata
from Cap de Creus canyon, NW Mediterranean by Orejas
et al. 2011b). Growth rates observed in aquaria for NW
Mediterranean M. oculata are higher when corals are fed five
times a week with a mixed diet of Mysidacea, frozen Cyclops
and Artemia salina nauplii (Orejas et al. 2011a) compared to
growth rates of corals fed three times a week with A. salina
nauplii only (Lartaud et al. 2013). Temperature and pH are
also important parameters that can affect growth rates, with
distinct responses depending on the species or local habitat
conditions (cf. details from Sect. 36.6 of this chapter, as well
as chapters by Reynaud and Ferrier-Pagès, this volume;
Maier et al., this volume; and Movilla, this volume).
Sediment accumulation stress slows coral growth, as seen
for L. pertusa from south Norway (Larsson et al. 2013). The
authors suggest that lower growth is likely due to the addi-
tional energy for polyps to clean themselves which decrease
the energy available for feeding, or to a lower polyp exten-
sion to reduce abrasion risk by sediment particles, limiting Fig. 36.7 (a) Skeleton cementation between Lophelia pertusa and
Madrepora oculata corals from the Gulf of Lion (Lacaze-Duthiers can-
ion exchanges from the environment to extracellular medium yon). (b) M. oculata (white arrow) growing on the wall of two living L.
(i.e., the area where mineralisation occurs). Anthropogenic pertusa polyps. Scale bar:1 cm. (Photographs © F. Lartaud (Sorbonne
pollutants such as drill cuttings can create a similar stressor University))
Sponges and fungi that attack dead coral parts at the base of cation of mediterranean intermediate waters combined with
the reef tend to form coral rubble by bioerosion. Rubble also change in nutrient supply and deoxygenation could affect the
contributes in reef formation by providing a substratum for capacity of CWCs to maintain growth rates (Cordes et al.
new larvae settlement (Roberts et al. 2009). 2016). Predictive habitat modelling approaches and global
Colony extension occurs over the whole lifespan of the datasets of key environmental parameters (e.g. temperature,
coral, and it is supported by the long lifespan of some reef- salinity, dissolved O2 and nutrients), are suggesting changes
building species. Radioisotope measurements reveal that the in the distribution of suitable habitats for CWC taxa in future
age of a 40 cm high L. pertusa colony from the NE Atlantic climate scenarios (IPCC 2014), though there are still large
can be up to 250 years (Pons-Branchu et al. 2005). This uncertainties in these approaches (Davies and Guinotte
means that a 2–3 m high colony needed several centuries to 2011). The spatial resolution and accuracy of these models
reach this size. However, lifespan differs depending on the are still largely insufficient to anticipate responses due to
species and/or the environment as a 45 cm high M. oculata short-term changes in local conditions (e.g. recovery times
colony from Norway has been estimated to be ~40 years old after physical disturbance, fluctuations of environmental fac-
(Sabatier et al. 2012). Nevertheless if sedimentation takes tors and feeding constraints). According to future predicted
place at a slower rate than coral growth, colony growth and climate IPCC-A2 scenario (IPCC 2014), the average tem-
colonisation by additional coral larvae in the dead or living perature for the deep Mediterranean Sea may increase by
part of the reef contributes to maintain reef formation over 1.5 °C by the end of the twenty-first century with an increase
very long periods. The oldest L. pertusa reef found to date is of 0.23 for salinity (Somot et al. 2006). Together with the
estimated in 8600 years old and it is located in Norwegian increase of temperature, pH will decrease as a result of
waters (Hovland and Mortensen 1999). anthropogenic CO2 absorbed by seawater. In the future (year
Reef growth is divided into five stages, corresponding to: 2100) Mediterranean deep waters, the pH change is esti-
(1) reef initiation, (2) framework expansion, (3) framework mated to be between −0.005 and −0.06 units (Palmiéri et al.
collapse, (4) partial burial of the coral rubble by superficial 2015). The local enhancement of acidification (e.g. due to an
sediments, and (5) finally possible larval recruitment on the increase in organic matter remineralisation) and associated
coral rubble depending on the environmental conditions, cumulative stressors yet constitute potential threats to CWCs.
allowing the formation of a geological structure induced by Consequences of climate change for Mediterranean
cyclic alternation of these different phases (Douarin et al. CWCs and their associated communities have to be evalu-
2014). The cyclic stages are facilitated by climatic evolution ated. Details on this topic are given by Maier et al. (this vol-
(e.g., glacial/interglacial cycles) allowing formation of coral ume) and Movilla (this volume).
carbonate mounds over thousands of years (Roberts et al.
2006). The present-day CWC reefs in the Mediterranean Sea
were initiated at the Late Pliocene/Early Pleistocene (Taviani 36.6.2 Impact of Temperature
et al. 2005, this volume). Depending on the area, reef forma-
tion may have been interrupted for long periods inducing Physiological behaviour of scleractinian CWCs have been
temporary extinction of CWCs in the eastern Mediterranean monitored in aquaria under different thermal conditions.
Sea during the early to middle Holocene from 11.4 to 5.9 kyr Long-term (12 months) aquaria experiments on Lophelia
BP linked to low oxygen conditions (Fink et al. 2012). pertusa from the Atlantic Ocean do not show absolute
changes in calcification rates under seawater temperatures of
9 °C and 12 °C (Hennige et al. 2015). Lophelia pertusa and
36.6 G
rowth in the Future Mediterranean M. oculata from the Mediterranean Sea however revealed
Sea species-specific growth rate responses with similar calcifica-
tion rates at 9 °C and 12 °C for L. pertusa, but lower rates at
36.6.1 Potential Influence of Climate Change 9 °C for M. oculata. At 6 °C, both species show low calcifi-
on the Mediterranean CWCs cation rates (Naumann et al. 2014). Similarly, calcification of
Dendrophyllia cornigera from the Menorca Channel
It is estimated that >80% of global warming over the last decreases from 12 to 8 °C (Gori et al. 2014).
40 years has been taken up by the oceans and penetrated to Thermal acclimation of calcification processes is well
depths of at least 700 m (Barnett et al. 2005). Among other established for a number of temperate and tropical sclerac-
anthropogenic stressors, the imprint of climate change on tinian coral species and the optimal temperatures for several
deep and intermediate Mediterranean waters is expected to species have been determined. However, for scleractinian
generate specific threats to CWC habitats, such as in canyons CWCs the thermal optimum and the potential for adaptation
or seamount flanks (see Ramirez-Llodra et al. 2010; Levin to temperature changes are still unknown. In situ and aquaria
and Le Bris 2015). The combination of warming and acidifi- experiments suggested that the upper lethal temperature for
L. pertusa from the Gulf of Mexico is near 15 °C (Brooke 2015; Gori et al. 2016), although some studies report an
et al. 2013). Freiwald et al. (2004) suggested that scleractin- expected higher sensititvity of L. pertusa and D. cornigera
ian CWCs, which occur less frequently in the Mediterranean species (Movilla et al. 2014b). McCulloch et al. (2012) esti-
Sea than in Atlantic and Pacific oceans, are at the uppermost mated that the energetic cost associated with pH up-regula-
of their thermal tolerance range in the Mediterranean tion was ~10% per 0.1 pH unit decreases in seawater. A
(14 °C). Considering this optimal range, it would be recent study suggests that a small fraction (<3%) of the total
expected that growth experiments conducted at tempera- energy demand is required for M. oculata calcification,
tures higher than 13 °C, should display a decline in the cal- allowing corals from the Adriatic Sea to maintain growth
cification rate for CWCs. However, not all CWC species rates in more acidic waters even under low feeding condi-
follow this rule as the calcification of D. cornigera from the tions (Maier et al. 2016).
shallow part of the Menorca Channel (~200 m) increases The synergic effect of temperature and ocean acidifica-
when temperature rises from 12 to 16 °C (Gori et al. 2014). tion has been recently tested and the first results suggest that
Desmophyllum dianthus from a deeper location in the crystallographic and molecular-scale bonding organisation
Adriatic Sea (430 m) shows significant decreases in calcifi- rather than calcification rate of L. pertusa from NE Atlantic
cation rates when exposed for a long period (8 months) to are affected by thermal and pCO2 changes (Hennige et al.
15 °C waters (Gori et al. 2016); this might be linked to the 2015). Nevertheless, additional studies providing informa-
decline in activity of enzymes involved in calcification (e.g., tion on the main sources of energy metabolised are required,
carbonic anhydrase). Reef formation in the future as highlighted by results from Gori et al. (2016) on D. dian-
Mediterranean may be dramatically affected by global thus from the Adriatic Sea.
warming or, assuming the different thermal tolerances of As this volume includes two chapters (already mentioned
species (e.g. D. cornigera exhibits a metabolism more effi- in this text) dealing with effects of ocean acidification in
cient at higher temperature, Gori et al. 2014), an increase in CWCs, no more details on this topic will be included in this
temperature may contribute to a shift in Mediterranean section.
CWC community composition. Analyses of fossils
(Wienberg et al. 2009) and recent corals from the Atlantic
(Keller and Os’kina 2008) suggest a higher temperature tol- 36.6.4 Impact of Oceanographic Conditions
erance of M. oculata compared to L. pertusa. Additionally, on the Growth of CWCs: The Case Study
scleractinian deep-water corals (Dendrophyllia sp. and of Dense Water Shelf Cascades
Eguchipsammia fistula) have been found in the Red Sea at in the Mediterranean Sea
temperatures exceeding 20 °C, leading to a revisiting on the
main persistence and resilience concepts for CWCs (Roder In the Mediterranean Sea, different areas (Aegean Sea,
et al. 2013). If the future baseline temperature changes in Adriatic Sea, Catalan Margin, Creta Island, Gulf of Lion) are
the deep Mediterranean provinces, questions regarding influenced by episodic dense water shelf cascades driven by
acclimation of Mediterranean corals have to be addressed. wind-induced conditions (Canals et al. 2006). These dense
D. cornigera from Cap de Creus canyon, NW Mediterranean, water plumes that overflow the shelf edge are associated with
and D. dianthus from south of Malta, tolerate elevated tem- significant decreases in temperature, significant increases in
peratures (17.5 °C) during 3 months in aquaria, showing the current speed and they may transport of large amounts of
higher growth rates for D. cornigera when temperature coarse sediment and organic matter (Palanques et al. 2006;
increases, which suggests that those species may be more Heussner et al. 2006; Canals et al. 2006). The precise effects
capable of surviving in warmer environments than previ- of cascading on CWC communities are not well documented
ously thought (Naumann et al. 2013). (but see Puig and Gili, this volume). As mentioned before, in
situ experiments showed a seasonal difference in the growth
patterns of M. oculata, which are suspected to result from
36.6.3 Ocean Acidification differences in the food availability induced by winter cascad-
ing events in the Lacaze-Duthiers canyon (Lartaud et al.
Acidification is known to alter growth rate of calcifying 2014). The expected scenario for the end of the twenty-first
organisms as global ocean composition becomes undersatu- century by the IPCC suggests a stronger stratification of the
rated in calcium carbonate. However, for scleractinian water column, which would result in a decrease of cascading
CWCs, long-term aquaria studies generally suggest that cal- events of at least 60%, compared to the present climate con-
cification of L. pertusa, M. oculata and D. cornigera colo- ditions (Hermann et al. 2008). Considering these preliminary
nies and D. dianthus solitary corals from the Mediterranean results, the effects of climate change could result in addi-
Sea are not affected by the pCO2 level projected at the end tional strong threats to the resilience of CWC reefs in the
of the century (Maier et al. 2013; Rodolfo Metalpa et al. Mediterranean Sea.
36.7 Conclusion References
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Sciences Doctoral Studies Programme is funded under the Programme Mineralogical Society of America and the Geochemical Society,
for Research in Third-Level Institutions Cycle-5 and co-funded under Washington, DC, 54:151–187
the European Regional Development Fund. Autun Purser is acknowl- Cölfen H, Antonietti M (2005) Mesocrystals: inorganic superstructures
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Demography and Conservation of Deep
Corals: The Study of Population 37
Structure and Dynamics
Lorenzo Bramanti, Giovanni Santangelo,
Maria Carla Benedetti, Mimmo Iannelli,
and Katell Guizien
Abstract of view, showing how this science evolved from the study
The science of demography was developed for the study of human populations to the conservation of animal popu-
of human populations, but the theoretical framework and lations. We then review the application of demographic
analytical techniques can be easily applied to animal pop- modeling to coral populations and in particular we focus
ulations, giving powerful instruments for conservation on the case study of the Mediterranean red coral
and management. Demography is then a paradigmatic (Corallium rubrum). This species is endemic to the
example of the advantages of interdisciplinary approaches Mediterranean Sea and besides it is not considered as a
which allow transferring the techniques developed in one cold-water coral species, it dwells in relatively cold envi-
field (e.g. human population studies) to different fields ronment and can be found at considerable depths.
(e.g. nature conservation and management). Cold-water
corals have been approached relatively recently by scien- Keywords
tist due to the technical constrains linked to the deep habi- Demography · Population dynamics · Corals · Cold-
tat where they live. However the fast development of water corals · Mediterranean Sea
underwater observation technologies is allowing to gather
data on those deep and not easily accessible ecosystems,
showing their paramount role in the ecosystem function-
ing. Due to the peace at which environmental changes are 37.1 D
emography: A Human Population
threatening natural ecosystems, increasing our knowledge Science
on cold-water corals is urgent and time constrained. Due
to the slow life cycles of the cold-water coral species, Demography is the science that studies populations, focusing
forecasting capacity is needed to understand the dynamics on their structure and their changes over time due to births,
of their populations. Demography can give this forecast- deaths, migration and aging.
ing capacity but, up to now, the paucity of data from deep To find the origins of demography we have to go long
coral populations still not allowed to apply demographic back in time. This science was born to study human popula-
models to those environments. Fortunately, the applications, to collect taxes and recruit men for military purposes.
tion of demographic models to other species with similar The main instrument for the collection of demographic data
characteristics can help a fast development of similar is the census. A census is the procedure of systematically
instruments to cold-water corals. The present chapter acquiring and recording information about the members of a
aims at introducing demography from an historical point given population. The first known census dates several thou-
sands years ago: with the appearance of the first states in the
Fertile Crescent and in Egypt, in the third millennium before
L. Bramanti (*) · K. Guizien
CNRS, Laboratoire d’Ecogéochimie des Environnements Common Era (BCE), the practice of registering people and
Benthiques (LECOB), Observatoire Océanologique, Sorbonne goods began, as an essential instrument of power to control
Universités, UPMC Univ Paris 06, Banyuls/Mer, France taxes and benefits (Frier 2000). Only the relevant data were
collected for this purpose and only when and where it was
G. Santangelo · M. C. Benedetti necessary. Censuses throughout antiquity then, were not
Dipartimento di Biologia, University of Pisa, Pisa, Italy
aimed at collecting global demographic information, but to
M. Iannelli establish the social position linked to wealth, or to generate
Dipartimento di Matematica, University of Trento, Povo, Italy

https://doi.org/10.1007/978-3-319-91608-8_37
424 L. Bramanti et al.
Fig. 37.1 (a) Exponential a Exponential population growth b Logistic population growth

population growth, also 7000 7000
known as Malthusian growth.
(b) Logistic population 6000 6000
growth. The growth rate
decreases as the population 5000 5000
N of individuals
reaches the maximum number
4000 4000
of individuals in a population
3000 3000
2000 2000
1000 1000
0 0
0 5 10 15 20 25 0 5 10 15 20 25
Year
lists for specific purposes: military cams, tribute collection, dynamics problems linked to the repopulation of earth after
corvees, food distributions (Scheidel 2007). Archeological big disasters (Bacaer 2010).
records suggest that Sumerians used to take censuses at The work of Euler and the subsequent consideration of
7 year intervals with the purpose of counting the number of Malthus represent a milestone in the field of population
people and livestock, as well as quantities of olive oil, butter, dynamics as they start to mathematically treat the dynamics
honey, milk, wool and vegetables (Kuhrt 1995). During the of the populations, passing from a description of the process
Roman Republic, censuses were taken regularly as a list, to to an attempt of forecasting. However, the dynamics
keep track of all adult males fit for military service, such as described are not realistic as they do not account for the limi-
for example the census ordered by roman emperor Caesar tation due to the environmental carrying capacity (i.e. the
Augustus, the first census made in Judea when it became a maximum population size that the environment can sustain
province of the Roman Empire and which record can be indefinitely, given resources available in the environment).
found in the New Testament (Luke 2:1–7, ESV). This limitation was solved by Pierre Francois Verhulst
In ancient times, demography was used only as an instru- (1838), who developed the logistic model describing a non-
ment to gather information on the number of citizens of a exponential population growth model characterized by a
country and was then reduced to a simple enumeration of decreasing rate as the population approaches a threshold
individuals and eventually of goods. When governments saturation level (Fig. 37.1b).
started to need information not only on the number of citi-
zens at the specific time of the census, but also on their future
number, demographic studies started to consider populations 37.2 Animal Demography
as dynamic entities.
Population dynamics is a branch of demography that Demographic models have been largely applied to simulate
studies populations as dynamic systems. The aim of popula- the dynamics of animal and plant populations. Derived from
tion dynamic studies is the understanding of mechanisms the logistic equation, the famous Lotka-Volterra multi-
driving changes in the number of individuals in a population equation model was independently developed by Volterra
and finally to give tools to forecast the number of individuals and Lotka, with the aim to describe the dynamics of non
in the future. human populations under intra and interspecific competitive
The need of forecasting capacity is linked to the applica- interactions (Volterra 1931). In 1957 Beverton and Holt
tion of models that consist in a simple mathematical repre- applied the logistic equation to fishery, proposing the yield
sentation of reality. The simplest demographic models take per recruit model, which represents the sustainable yield of
the name from Thomas Robert Malthus, which in 1798 dis- a fish population as a function of both individual growth and
cussed the infinite human population growth (Fig. 37.1a). mortality (Beverton and Holt 1957). Since the Beverton-Holt
Despite the concept of infinite population growth is linked to model, demographic approaches have been frequently
Malthus (malthusian growth), the first mathematical formali- applied to the conservation of marine species (e.g. Gerber
sation is due to Euler, which in 1748 (50 years before et al. 2005; Rossi et al. 2017a, b), and population models are
Malthus) published a essay entitled “Introduction to Analysis now a common instrument for marine ecologists. In the last
of the Infinite” where he dealt about human population decades scientists started to apply different families of mod-
els other than the ones derived from the logistic equation. In
37 Demography and Conservation of Deep Corals 425
particular matrix population models have been frequently S1 S2 Sn

applied due to their capacity of dealing with long-lived
species.
RECRUIT X1 X2 Xn
37.2.1 Matrix Population Models

b2
Population dynamic models based on transition matrices
bn
have been applied to a variety of organisms and they revealed
to be a powerful instrument in conservation and management X = Age-size class
of structured populations of long-lived species. Advices for S = Survival rate
the conservation measures of several marine species derived b = Reproductive rate
from the results of this family of models. The Mediterranean

Fig. 37.2 Conceptual model representing the dynamics of a stage
red coral (Corallium rubrum) is a paradigmatic example of structured population. Each stage (circle) is linked to the previous
this direct relationship between modeling and conservation: through survival probability (Sx) and the first stage (recruitment) is
the ban of harvesting with trawling techniques, as well as the linked to the fecundity of the reproductive stages bx)
ban of harvesting shallower than 50 m depth, were decided
by FAO on the basis of demographic studies (Santangelo and defined time; in particular, for example, under the assump-
Bramanti 2006; Tsounis et al. 2013). Other species, tion of “steady state” mortality can be calculated as the dif-
characterized by long life cycles, have been the object of ference between the number of individuals in one age class
demographic studies based on matrix population models; as or vital stage and that in the following (younger) one. A
examples we can find cetaceans, with models applied to the population is considered in steady state if the ratio between
study of the right whale (e.g. Fujiwara and Caswell 2001), two following classes remains constant overtime (i.e. a pro-
the fin whale (e.g. Arrigoni et al. 2011) and the killer whale portional mortality occurs; Caswell 2001). In this case, age
(e.g. Brault and Caswell 1993). Sea turtles as well as polar classes distribution follows a monotonic, decreasing pattern
bears have been object of population dynamics modeling (olds are less numerous than young).
studies (e.g. Crouse et al. 1987; Molnár et al. 2014). Not only The graphical representation of a conceptual model for
vertebrates are object of demographic studies. In marine the dynamics of an age-structured population is shown in
environment, corals are long-lived species whose population Fig. 37.2. The graph represents the dynamics of the popula-
dynamics can be modeled with matrix population models. tion highlighting the role of the different life history traits.
The topic of coral demography will be more extensively The dynamic relationships between the different classes or
treated in the Sect. 37.2.3 (Coral demography). vital stages are described by a Markov chain in which sur-
Matrix population models have been introduced to vival probability Si links the number of individuals in one
describe the dynamics of structured populations. In such class to that in the subsequent class, while recruitment is
populations, individuals are classified in categories based on linked to population reproductive output bi (Fujiwara and
their demographic traits. One of the most important traits is Caswell 2001). Population dynamics are then described
age, which allows a temporal resolution of the model mathematically in the form of a recurrence equation in
(Bramanti et al. 2015). Age structured models were firstly set which the iteration of a transfer matrix allows to project the
out by Lewis (1942) and Leslie (1945, 1948) in their seminal structure of the population overtime. Population trend will
works on population dynamics, but some other characteristics depend on the leading eigenvalue of the transfer matrix,
such as size, life cycle stage etc., can be used, depending on population growth occurring when the latter is larger than 1
the question. A comprehensive description of matrix (Caswell 2001).
population models and their properties have been given by
Caswell (2001).
Objective of a matrix population model is to project the 37.2.2 Metapopulation Models
structure of a given population along time under the
conditions imposed by the model. In order to project the The model of Fig. 37.2 is based on the assumption of “closed
structure of a population all the data necessary to describe populations”, where recruitment is linked to local
the present structure of the population as well as the basic reproduction. In an “open” population, local reproduction
data on the life history traits driving its dynamics (e.g. and local recruitment are not univocally linked. This means
reproductive and survival rates) have to be collected. that local population dynamics approach should be replaced
Population data are organized in static “life-tables” which by a meta-population approach at the scale where a set of
contain the basic information on the population structure in a populations form a closed network (Fig. 37.3). The closed
proceeding from each population within the population’s

network which will balance the local mortality between two
reproductive events (Hastings and Botsford 2006).
The mathematical description of this meta-population
model is similar to a model for age-structured population by
a recurrence relationship based on a transition matrix
redistributing offspring in space, and meta-population
viability is determined by the leading eigenvalue of the
transition matrix being larger or equal to 1. For long-lived
species with fecundity proportional to age and dispersing life
stage, such as corals, the two transition matrices can be
combined in an age-structured meta-population model, as
done by Guizien and Bramanti (2014) for the Mediterranean
red coral (see Sect. 37.3.1.4: connectivity matrix for more
details).
Fig. 37.3 Meta-population conceptual model. Circles represents pop-
ulations. Each population has its own dynamics (round arrows) and
exchange individuals with other populations (straight arrows) 37.2.3 Coral Demography
network (i.e. meta-population) is defined by the populations Corals are among the most long-lived marine species (Roark
among which exchange of individuals happens (i.e. et al. 2006; Lartaud et al. 2017) and they form structured
colonisation). populations composed by individuals of different ages.
The early meta-population model of Levins (1969) Being sessile animals, corals can disperse only during a
described the presence / absence of a species in a set of restricted period of time (each year) in form of pelagic eggs
similar patches, assuming the same rate of extinction and the or lecitotrophic larvae (planulae). Despite clonal propagation
same level of connectivity for every patch. In such a network, has been observed in some species (Highsmith 1982; Lasker
species persistence occurred only if colonisation was larger 1990), dispersal is mainly linked to the larval phase due to
or equal to local extinction. By making explicit the variation the low dispersal capacities of coral fragments.
of colonisation with geographical distance and surface area Population dynamic models have been applied to tropical
of patches, Hanski and Ovaskainen (2000) formulated a and temperate coral species to project the evolution of their
spatially structured meta-population model describing the demography in time. The first studies derive from the semi-
probability of patch occupation according to patches distance nal work of Hughes (1984) and are focused on tropical spe-
and surface for a species with uniform colonisation and cies (e.g. Hughes and Jackson 1985; Bak and Meesters
extinction probability. However, such approach is useful 1998; Edmunds and Elahi 2007; Bramanti et al. 2015).
only for mobile species, which displacement results from a Projections can be used either with forecasting purposes
tradeoff between energetic reserve and motion cost, such as (i.e. anticipating the changes in population structure under
terrestrial mammals, on the contrary, it is not useful for different scenarios) or with description purposes (i.e. for
species dispersing in a restricted period of the life cycle in understanding the functioning of the studied population;
form of oocytes or larvae, such as corals. In the ocean, where Shannon 1975).
the flow is anisotropic (variable according to the direction it In temperate seas, several works on coral population
is measured), eggs and larvae transport is spatially structured dynamics have been focused on species dwelling in relatively
and colonisation among a set of populations vary according shallow environments (e.g. C. rubrum, Paramuricea clavata,
to the location of source and sink populations. The transfer Balanophyllia europaea) assuming closed populations
rates within a marine meta-population are therefore described maintaining themselves through self-recruitment (Santangelo
by spatially explicit connectivity matrices resulting from et al. 2007; Bramanti et al. 2009; Linares et al. 2010; Caroselli
ocean current transport and specie-specific larvae motility et al. 2012). The preferential application to shallow
behavior (e.g. Katz et al. 1994; Guizien et al. 2006; Luiz populations is dictated by the intrinsic characteristics of
et al. 2013). In a spatially explicit discrete meta-population matrix models which are high data demanding. In order to
model, connectivity matrices are combined with data on the apply a matrix population model, in fact, data on several life
fecundity of source populations and data on the recruitment history traits are required, such as population density, colony
success in sink populations. The objective is to describe the growth rates, population structure, reproductive output and
redistribution of the meta-population reproductive output mortality.
37.3 Mediterranean Corals Mediterranean Sea several species of deep, not reef forming
species are present which can form millennial underwater
The world “coral” immediately recall images of colorful forests (Fig. 37.6). Coral gardens formed by Callogorgia
tropical coral reefs in shallow crystal waters. However, it is verticillata, Antipathella subpinnata and Parantipathes larix
now widely known that coral bioformations are not exclusive as well as dense and pristine forest of the black coral
of shallow tropical waters (Fig. 37.4). Massive biogenic Leiopathes glaberrima and the bamboo coral Isidella
formations mainly composed by corals (i.e. deep coral reefs) elongata have been found in the Sardinian waters (Bo et al.
have been found in deep, dark, cold, nutrient-rich waters, 2015; Cau et al. 2017a, b; Bo and Bavestrello, this volume;
also at not tropical latitudes. These formations are known as Rueda et al., this volume; Altuna and Poliseno, this volume;
cold-water corals (CWCs) and can occur in fjords, along the Chimienti et al., this volume) as well as in Maltese waters
edge of the continental shelf and around offshore submarine (Deidun et al. 2015; Knittweis et al., this volume). Forests of
cliffs and seamounts at almost all the latitudes (Freiwald the gold coral (Savaglia savaglia) have been reported from
et al. 2004, 2009, 2017; OSPAR 2015; Freiwald and Roberts the southern Tyrrhenian Sea (Cerrano et al. 2010).
2005; Roberts et al. 2006, 2009; Altuna and Poliseno, this
volume). CWC, similarly to tropical corals, form three-
dimensional biogenic structures (the so called animal for- 37.3.1 Matrix Models for Conservation:
ests; Fig. 37.5 sensu Rossi et al. 2017a, b), but unlike tropical The Case Study of the Mediterranean
reef species, CWC do not host symbiotic algae in their pol- Red Coral (Corallium rubrum)
yps and consequently, for their survival they do not depend
on sunlight, but on the capture of seston from the surround- Due to the difficulty of data collection on deep dwelling spe-
ing water (Duineveld et al. 2004; Thiem et al. 2006). cies, none of the deep CWC has been object of demographic
The CWCs are not only restricted to reef forming sclerac- modeling, with the exception of the Mediterranean red coral
tinian species (e.g. Lophelia pertusa and Madrepora ocu- (Corallium rubrum) which although is not a “true” CWC,
lata). The so called deep coral gardens occupy huge areas in can be found in relatively deep (800 m, Costantini et al.
which octocorals dominate: species belonging to Alcyonacea, 2010) and cold (<12 °C) environments. Due to its wide
Pennatulacea and Anthipataria, for example, have been bathymetric range (populations of this species can be found
found at high densities in the UK waters (Lancaster 2014) as shallow as 10 m depth Rossi et al. 2008) and its economic
and Gulf of Mexico (Quattrini et al. 2014). Also in the importance (Tsounis et al. 2010) it has been object of accu-
Fig. 37.4 Tropical coral bioformation. Moorea, French Polynesia. (© Lorenzo Bramanti, LECOB-CNRS)
Fig. 37.5 CWC bioformation

composed by Madrepora
oculata at 325 m depth in the
Lacaze-Duthiers canyon
(North western Mediterranean
sea). Distance between the
two laser beams is 6 cm. (©
UPMC-Fondation TOTAL)
Fig. 37.6 Leiopathes

glaberrima from
Mediterranean sea. (©
Alessandro Cau, University of
Cagliari)
Fig. 37.7 Mediterranean red

coral (Corallium rubrum)
shallow population (30 m
depth) at Cap de Creus
(Spain). (© Francisco
Romero)
rate demographic studies (Garrabou and Harmelin 2002; Abbiati 2001; Cau et al. 2016; Garrabou et al. 2017). Despite
Santangelo et al. 2007; Bramanti et al. 2009, 2014, 2017; those changes, data on shallow water populations have been
Priori et al. 2013; Santangelo et al. 2015). useful to develop matrix population models to project popu-
Corallium rubrum is distributed throughout the lation structure over time under human (harvesting) and
Mediterranean Sea and neighboring Atlantic rocky shores environmental (climate change) disturbances (Bramanti
between 10 and 800 m depth (Costantini et al. 2010). It is an et al. 2017). The model helped researchers in understanding
extremely long-lived species which life span can overcome the main drivers of deep and shallow population dynamics
one century (Garrabou and Harmelin 2002; Priori et al. (Bramanti et al. 2009) and should help in planning conserva-
2013). Harvested and traded since thousands of years due to tion measures (Santangelo et al. 2015). Moreover, the results
the use of its red carbonatic skeleton in jewelry industry of the projections have been recently validated by direct
(Jimenez and Orejas 2017), C. rubrum is a paradigmatic observations on deep populations (Cau et al. 2016).
example of an overexploited species (Tsounis et al. 2010 and Here we present an example of the steps followed in the
references herein). The General Fishery Commission for the development of a matrix population model for a closed popu-
Mediterranean (GFCM) highlighted the necessity to forecast lation of C. rubrum dwelling in the shallower portion of the
the structure of the most endangered populations of this spe- species bathymetric range in the NW Mediterranean Sea
cies under harvesting scenarios in order to plan management (Fig. 37.7; Santangelo et al. 2007). To describe the life history
and conservation actions (GFCM 2011). traits of the population, a “life table” has been compiled. The
Hundreds of years of harvesting (Tsounis et al. 2010) “life–table” summarizes the data on size/age structure (num-
likely brought to the alteration of the structure and density of ber of colonies in each size/age class), survival and fecundity
the shallow populations of C. rubrum (Santangelo and (number of larvae produced per colony of each class).
Fig. 37.8 Fecundity
estimation. (a) Polyps of
Corallium rubrum. (b)
Mature oocytes found inside
one of the polyps
37.3.1.1 Fecundity et al. 2013; Bramanti et al. 2014). Colony age was estimated
Fecundity (number of larvae produced per individual) is a on a subsample of colonies of different size, applying the
key trait of a population, as it allows to link the present organic matrix staining method (OMS), proposed by
structure of the population to its reproductive output. In Marschal et al. (2004) and validated by Gallmetzer et al.
many cases values of fecundity cannot be directly measured (2010) and Benedetti et al. (2016). The relationship between
and have to be estimated on the basis of other measurable age and size was then used to divide a larger sample of
traits such as fertility (% of fertile colonies), number of colonies in size/age classes based on the measured diameter.
mature oocytes and / or immature planulae per female polyp, Although de facto the model for the red coral is based on
number of polyps per colony and sex ratio (Santangelo et al. size classes, we use the growth rate to estimate the most
2003; Priori et al. 2013). The main difficulty in this procedure probable age of colonies in each size class and the width of
is due to the need of a minimum number of mature colonies the size class that can be transitioned with the growth
that have to be sampled just before larval release. Moreover, occurring in a defined time period. This last aspect is a
the number of larvae released is estimated on a subsample of fundamental and necessary information for the demographic
the polyps of the colony (Fig. 37.8). Alternatively, fecundity model as it allows to determine the time unit of the projec-
can be directly quantified on colonies maintained in aquaria, tion interval.
as it has been done in the case of Pocillopora damicoris Due to the extremely long life cycle of the species, which
(Bramanti et al. 2015) and C. rubrum (Martínez-Quintana can overcome one century, it is not possible to follow the fate
et al. 2015), where female colonies are isolated in different of a single cohort along its life span. For this reason, a static
aquaria during the spawning period and the released larvae “life table” (sensu Ricklefs and Miller 2000) was set out.
are counted. The advantage of this method is that the number The analysis of the frequency distribution of size-age
of larvae released is directly counted and not estimated. The classes performed in different years showed that population
drawback is that the colonies have to be maintained in size-age structure exhibits a monotonic, regularly decreasing
aquaria and fecundity can be measured only on a limited trend (Fig. 37.9; Santangelo et al. 2007; Bramanti et al.
number of colonies. 2014), suggesting that the populations were in steady state
(i.e. proportional life stages, Caswell 2001). To estimate
37.3.1.2 Colony Growth and Survival survival/mortality, therefore, the ratio between the number of
For the application of a matrix model, populations are individual present in an age class and the number of
divided in classes. Classes can be represented by demographic individual present in the following age class was used. For
traits such as life stage (e.g. right whale; Fujiwara and each size-age class, this ratio represents the probability of
Caswell 2001) or size (e.g. Porites astreoides, Diploria survival of the colonies in the passage from 1 year to another.
strigosa and Paramuricea clavata; Edmunds 2010; Linares
et al. 2008 respectively). In the case of C. rubrum, the 37.3.1.3 Recruitment
populations have been divided in size/age classes according To develop the demographic model, larval success has been
to the relationship found between colony size (basal calculated as the proportion of larvae surviving until
diameter) and colony age (Santangelo et al. 2007; Priori settlement. Under the assumption of closed populations (no
1000 individuals in the populations forming the network (Wilson

and Rannala 2003). However, this method includes part of
the fate of a larva after it reaches its destination, namely
800 recruitment and survival until the age it was sampled for
genotyping. Hence, ideally, this method requires sampling
recruits only, solving in this way, the problem of the
N of individuals
600 unknown recruitment success, but it has not been imple-

mented yet. On the other hand, transfer rates can be esti-
mated from larval transport, on the basis of biophysical
400
models integrating ocean current and larval traits (Guizien
et al. 2006; Cowen and Sponaugle 2009; Butler et al. 2011;
Luiz et al. 2013). The interest of this latter method lies in its
200
forecasting potential: if ocean current changes (for instance
with climate change) changes in larval transport can be pre-
0 dicted. The limitation of this method lies in the gap of
1 2 3 4 5 6 7 8 9 10 11 12 13 knowledge on larval traits (such as spawning period,
size/age class spawning duration, pelagic larval duration, and motility
behavior) for many deep coral species (but see Brooke and
Fig. 37.9 Size/age structure of a Corallium rubrum shallow popula- Young 2005; Larsson et al. 2014) In particular, motility
tion. (Reprinted from Santangelo et al. (2007), Copyright (2007), with behavior is decomposed in a passive part defined by the
permission from Elsevier)
larval buoyancy (in general negative resulting in a sinking
behavior) and an active part defined by larval swimming
input from other populations), recruitment success is the activity rate and swimming speeds which can compensate
ratio between observed recruits and number of larvae or outcompete sinking at the expenses of energy loss. For
produced by the population. A recruit is defined as a new C. rubrum, the larval motility behavior has been quantified
individual added to the population. Recruitment is the first and resulted unexpectedly highly active (taking into
age class of the population and the number of recruits account that larvae are lecitotrophic) leading to an upward
depends yearly on the fecundity and, in case of density larval motion despite the negative buoyancy of the larvae
dependent recruitment, on the density of adults. For these (Martínez-Quintana et al. 2015). In the Mediterranean Sea,
reasons larval success is not a fixed number but it changes a connectivity matrix approach to metapopulation model-
according to adult density (Santangelo et al. 2007; Bramanti ing has been applied to C. rubrum by Guizien and Bramanti
et al. 2009, 2015). For the development of C. rubrum demo- (2014). Results suggested that connectivity can affect pop-
graphic model, recruitment has been estimated both on natu- ulation structure, suggesting that this species is organised
ral and artificial substrates (Bramanti et al. 2005, 2014; in a metapopulation framework, at least at the scale of the
Santangelo et al. 2012). Gulf de Lion.
In the case of open populations, recruitment success can-
not be known from observations and should be estimated
from experiments. For example introducing a known number 37.4 Conclusive Remarks
of larvae in controlled conditions and quantify the percent-
age of settled larvae. The percentage of settled larvae sur- Despite the importance of a modeling approach for conser-
vival will allow estimating the recruitment success, bearing vation, demographic models have still not been developed
in mind that it will be always overestimated due to the impos- for CWC species, mainly due to the technical difficulties of
sibility to quantify predation rate in laboratory conditions. sampling in deep environment. The Mediterranean red coral
(Corallium rubrum) represent an exception as it have a wide
37.3.1.4 Connectivity Matrices bathymetric range (10–800 m; Costantini et al. 2010) and
When populations form a network, offspring produced in shallow populations are easily accessible to SCUBA divers.
each population are redistributed among them by a connec- For this reasons, C. rubrum has been object of detailed
tivity matrix that upscales dispersal of individual larvae at demographic studies which resulted in the development of
the meta-population scale. Connectivity matrices contain- population dynamic models based on transition matrices
ing transfer rates of individuals between source and sink (Santangelo et al. 2007; Bramanti et al. 2009). The model
populations can be established in two ways. On one hand, developed for shallow populations has been used to explain
transfer rates can be estimated from contemporary gene some characteristics of deep populations structure and
flow, based on the analysis of genetic similarity between dynamics (Bramanti et al. 2009, Cau et al. 2016), however its
capacity to forecast the dynamics of deep populations in a Bacaer N (2010) A Short history of mathematical population dynam-
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Heidelberg, pp 691–700 ciated fauna in the Mediterranean Sea and adjacent areas
Cold-Water Coral in Aquaria: Advances
and Challenges. A Focus 38
on the Mediterranean
Covadonga Orejas, Marco Taviani, Stefano Ambroso,

Vasilis Andreou, Meri Bilan, Marzia Bo, Sandra Brooke,
Paal Buhl-Mortensen, Erik Cordes, Carlos Dominguez-
Carrió, Christine Ferrier-Pagès, Antonio Godinho,
Andrea Gori, Jordi Grinyó, Cristina Gutiérrez-Zárate,
Sebastian Hennige, Carlos Jiménez, Ann I. Larsson,
Franck Lartaud, Jay Lunden, Cornelia Maier,
Sandra R. Maier, Juancho Movilla, Fiona Murray,
Erwan Peru, Autun Purser, Maria Rakka,
Stéphanie Reynaud, J. Murray Roberts, Pedro Siles,
Susanna M. Strömberg, Laurenz Thomsen, Dick van
Oevelen, Alfredo Veiga, and Marina Carreiro-Silva
Abstract reproduction and physiology, which can be approached in

Knowledge on basic biological functions of organisms is situ or by collecting specimens and rearing them in aquaria,
essential to understand not only the role they play in the is particularly challenging for deep-sea organisms like
ecosystems but also to manage and protect their popula- cold-water corals. Field experimental work and monitoring
tions. The study of biological processes, such as growth, of deep-sea populations is still a chimera. Only a handful of
C. Orejas (*)
Instituto Español de Oceanografía (IEO), Centro Oceanográfico de
Baleares, Palma de Mallorca, Spain S. Brooke
e-mail: [email protected] Florida State University Coastal and Marine Laboratory,
St. Teresa, FL, USA
M. Taviani
Institute of Marine Sciences (ISMAR-CNR), Bologna, Italy P. Buhl-Mortensen
Institute of Marine Research, Bergen, Norway
Woods Hole, MA, USA E. Cordes · J. Lunden
Biology Life Sciences Building, Temple University,
Philadelphia, PA, USA
S. Ambroso · C. Dominguez-Carrió · A. Gori · J. Grinyó
C. Ferrier-Pagès · S. Reynaud
Institut de Ciències del Mar (CSIC), Barcelona, Spain
Département de Biologie Marine,
V. Andreou Equipe d’Ecophysiologie, Centre Scientifique
Enalia Physis Environmental Research Centre (ENALIA), de Monaco, Monaco, Monaco
Nicosia, Cyprus
C. Gutiérrez-Zárate · A. Veiga
M. Bilan · A. Godinho · M. Rakka · M. Carreiro-Silva Aquarium Finisterrae, A Coruña, Spain
IMAR – Institute of Marine Research, University of the Azores,
S. Hennige · F. Murray · J. M. Roberts
Horta, Azores, Portugal
University of Edinburgh, School of Geosciences,
MARE – Marine and Environmental Sciences Centre, Edinburgh, UK
Horta, Azores, Portugal
C. Jiménez
OKEANOS – Center of the University of the Azores, Enalia Physis Environmental Research Centre (ENALIA),
Horta, Azores, Portugal Nicosia, Cyprus
M. Bo Energy, Environment and Water Research Centre (EEWRC)
Università degli Studi di Genova, Genova, Italy of The Cyprus Institute, Nicosia, Cyprus

https://doi.org/10.1007/978-3-319-91608-8_38
research institutes or companies has been able to install in dures are valuable to any researcher interested in conduct-
situ marine observatories in the Mediterranean Sea or else- ing experimental work with cold-water corals in aquaria. It
where, which facilitate a continuous monitoring of deep- was impossible to include contributions from all laborato-
sea ecosystems. Hence, today’s best way to obtain basic ries in the world currently working experimentally with
biological information on these organisms is (1) working cold-water corals in the laboratory, but at the conclusion of
with collected samples and analysing them post-mortem the chapter we attempt, to our best of our knowledge, to
and / or (2) cultivating corals in aquaria in order to monitor supply a list of several laboratories with operational cold-
biological processes and investigate coral behaviour and water coral aquaria facilities.
physiological responses under different experimental treat-
ments. The first challenging aspect is the collection pro- Keywords
cess, which implies the use of oceanographic research Azooxanthellate corals · Husbandry · Aquaria experi-
vessels in most occasions since these organisms inhabit mental work · Behaviour · Ecophysiology ·
areas between ca. 150 m to more than 1000 m depth, and Mediterranean Sea
specific sampling gears. The next challenge is the mainte-
nance of the animals on board (in situations where cruises
may take weeks) and their transport to home laboratories. 38.1 Aquaria Maintenance
Maintenance in the home laboratories is also extremely and Experimental Work with Cold-
challenging since special conditions and set-ups are needed Water Corals. From the Beginning
to conduct experimental studies to obtain information on to the Present
the biological processes of these animals. The complexity
of the natural environment from which the corals were col- 38.1.1 The Challenges of Mimicking
lected cannot be exactly replicated within the laboratory the Natural Environment
setting; a fact which has led some researchers to question
the validity of work and conclusions drawn from such Conducting experimental work with cold-water corals
undertakings. It is evident that aquaria experiments cannot (CWCs) in aquaria is a fairly recent research field. To our
perfectly reflect the real environmental and trophic condi- best knowledge, the first attempts to keep CWCs alive were
tions where these organisms occur, but: (1) in most cases conducted in 1980 when G.A.B. Shelton kept fragments of
we do not have the possibility to obtain equivalent in situ the reef-building CWC Lophelia pertusa in the Department
information and (2) even with limitations, they produce rel- of Zoology at the University of Oxford in order to study the
evant information about the biological limits of the species, behaviour of this coral (Shelton 1980). He was specifically
which is especially valuable when considering potential interested in the electrical conduction mechanisms underly-
future climate change scenarios. This chapter includes ing coral behaviour and coordination. In the laboratory, L.
many contributions from different authors and is envi- pertusa has been successfully reared in the facilities of
sioned as both to be a practical “handbook” for conducting Tjärno Marine Lab (University of Gothenburg, Sweden)
cold-water coral aquaria work, whilst at the same time since the late 1990s.
offering an overview on the cold-water coral research con- Eighteen after the initial work by Shelton, Mortensen and
ducted in Mediterranean laboratories equipped with aquaria Rapp (1998) studied the growth patterns of the same coral
infrastructure. Experiences from Atlantic and Pacific labo- species, maintaining colonies in aquaria with running seawa-
ratories with extensive experience with cold-water coral ter for more than 18 months in the Trondhjem Biological
work have also contributed to this chapter, as their proce- Station (Norwegian University of Science and Technology).
J. Movilla
A. I. Larsson · S. M. Strömberg
Instituto Español de Oceanografía, Centro Oceanográfico
Department of Marine Sciences – Tjärnö,
de Baleares, Estación de Investigación Jaume Ferrer,
University of Gothenburg, Strömstad, Sweden
Menorca, Spain
F. Lartaud · E. Peru
Instituto de Ciencias del Mar (ICM-CSIC),
Sorbonne Université, CNRS, Laboratoire
Barcelona, Spain
d’Ecogéochimie des Environnements Benthiques,
LECOB, Observatoire Océanologique, A. Purser
F-66650 Banyuls-sur-mer, France Alfred Wegener Institute, Helmholts zentrum
für Polar und Meeresforschung,
C. Maier
Bremerhaven, Germany
Laboratoire d’Océanographie de Villefranche (LOV),
Villefranche-sur-Mer, France P. Siles
C/ Alcalde de Mostoles 5, entlo, Barcelona, Spain
S. R. Maier · D. van Oevelen
Royal Netherlands Institute for Sea Research (NIOZ), L. Thomsen
Yerseke, The Netherlands Jacobs University, Bremen, Germany
38 Cold-Water Coral in Aquaria: Advances and Challenges 437
This pioneering work allowed obtaining the first ex situ data Purser 2011), or the effects of oil spills on these species
on this coral, contributing to increase our knowledge of a (DeLeo et al. 2016). The advances in rearing L. pertusa has
basic and fundamental aspect of the biology and ecology of also lead to a number of successful spawning seasons in the
a CWC species, spurring the modern era of experimental laboratory when embryo development and larval behaviour
CWC studies. Starting in 1999, P. Mortensen further devel- could be studied (Larsson et al. 2014; Strömberg and
oped methods for studying the growth and behaviour of L. Larsson 2017). The current chapter provides an overview of
pertusa in aquaria (Mortensen 2001); this work demon- the advances made on the maintenance and ex situ experi-
strated that it is possible to keep corals alive in closed water menting with CWCs, placing the focus in the Mediterranean
circulation systems for more than a month, and for more than region, but also adding integrative relevant experiences
a year with a continuous supply of seawater. Keeping L. per- from elsewhere.
tusa in aquaria for such a long period allows for controlled
experiments covering many aspects of its biology (e.g.
behaviour, physiology, growth and reproduction). 38.2 C
old-Water Coral Sampling
After these pioneer studies, the field rapidly evolved in and Maintenance on Board
the last two decades. Large advances have been achieved in
both the technical aspects regarding aquaria infrastructures This section presents an overview of different approaches
to maintain CWCs alive (e.g. Olariaga et al. 2009), and the used for CWC sampling as well as maintenance on board
development of specific experimental set-ups to investigate and transport to home laboratories. Some experiences on
particular aspects of the biology, physiology and ecology of short-term experiments on board are also included.
CWCs. The first years of the twenty-first century were par-
ticularly fruitful in this respect. Dodds et al. (2007) published
the first aquarium-based ecophysiology study on L. pertusa. 38.2.1 Cold-Water Coral Sampling
Dodds and her team conducted experiments to study the and Transport to Home Laboratories
respiratory physiology of L. pertusa under altered tempera-
ture and oxygen levels at the Scottish Association of Marine Over recent years several methods have been employed for
Science (SAMS), using aquaria infrastructures specially the collection of CWCs for maintenance and experimenta-
designed to maintain CWCs. The first results on growth rates tion, such as dredges, box-cores, grabs, remotely operated
of Mediterranean specimens of L. pertusa and Madrepora vehicles (ROV) and manned submersibles (e.g. Mortensen
oculata measured in aquaria were published in 2008 (Orejas 2001; Roberts et al. 2006; Brooke et al. 2009; Maier et al.
et al. 2008). That same year, Maier (2008) published the first 2009; Orejas et al. 2011; Taviani et al. 2011), as well as
work on the recovery capacity of L. pertusa in aquaria from through opportunistic sampling of corals accidentally cap-
tissue injuries. After these initial studies, several experimen- tured (as bycatch) in fishing vessels (e.g. Sampaio et al.
tal works on feeding ecology of CWCs were conducted with 2012). The collection of living CWC could be a relatively
different CWC species (e.g. Purser et al. 2010; Tsounis et al. “simple” operation, but the subsequent procedure of keep-
2010; Reynaud and Ferrier-Pagès, this volume; more details ing them alive on-board of the ship and their later safely
given in Sect. 38.5.2). transfer to a designated scientific aquarium can be a highly
During the last 15 years, advances in the experimental demanding task and needs appropriate preparation. It is gen-
approaches have increased exponentially. Several studies on erally acknowledged that more impacting methods such as
growth rates in aquaria of CWCs from the Mediterranean dredges can cause significant stress to the organisms (visi-
and elsewhere have been published (e.g. Maier et al. 2009, ble as increased mucus production, or polyp retraction for
2012; Orejas et al. 2011; Naumann et al. 2011, 2013; extended periods of time), and can cause severe damage to
Lartaud et al. 2013, 2014, this volume) as well as studies on coral tissue. Indeed, any method to collect living CWC from
the physiological response of CWCs to various experimen- their habitats unavoidably generates a profound stress on the
tal conditions (e.g. Gori et al. 2014a, 2015; Roik et al. 2015; coral polyps. Entire coral colonies or coral fragments are
Reynaud and Ferrier-Pagès, this volume). These studies suddenly and dramatically extracted from their habitat,
included experiments conducted under future IPCC reposed in canisters or analogue containers on the ROV or
(Intergovernmental Panel on Climate Change) scenarios of submersible, and exposed to changes in pressure and ther-
global warming and acidification (Maier et al. 2009, 2012, mal shocks during their journey from the seabed to the sur-
2013a, b, 2016, this volume; Movilla et al. 2014a, b, this face. The induced stress represents a significant loss of
volume; Carreiro-Silva et al. 2014; Hennige et al. 2015; energy, and can affect the survival of corals in captivity.
Gori et al. 2016, among others), as well as experiments car- Here we provide basic and practical information on how to
ried out to better understand the potential consequences of best maintain coral viability, largely derived from empirical
deep-sea drilling activities on CWC habitats (Larsson and experience (Box 38.1).
14 °C have been registered in the Ionian Sea and of 13 °C in

Box 38.1: Best Practice for Ship-Board Maintenance the Gulf of Lions). The geographic location of the
of CWC Mediterranean basin translates into considerably high sur-
Immediately after collection, corals should be trans- face temperatures, especially in summer months, typically
ferred with care to temperature-controlled aquaria filled the season when many oceanographic surveys are conducted.
with deep-sea water (collected with Niskin bottles from These issues must be taken into account when planning the
a CTD-Rosette or with a submersible water pump, for ship-board maintenance and later transfer of live CWCs.
instance). Coral maintenance on board may be pursued Minimising coral air exposure after collection is another
through sophisticated or less sophisticated systems, important factor, particularly when collecting gorgonians,
according to the situation. Whenever possible, the best because some species oxidise (become black) when
practice is to set-up a laboratory equipped with plastic exposed to air and die rapidly (e.g. Dentomuricea aff.
or glass containers filled with seawater maintained at meteor, Acanthogorgia spp.).
deep-sea temperature. Ideally, a closed system benefits Even for less sophisticated systems, some good planning
survival chances. Flow is maintained by recycling fil- is advisable. The maintenance of corals after collection may
tered seawater between the container and a chilling unit also be achieved either by temporarily storing them in on-
connected to a pump, with an aeration system. Handling board refrigerators or cold rooms at temperatures between
should be minimised as much as possible during the 10–12.5 °C for Mediterranean CWCs. As mentioned, seawa-
following weeks to allow corals to acclimate to aquar- ter for on board maintenance should be collected in advance,
ium conditions. Gently washing the corals with a small giving preference to ambient bottom seawater, rather than
water stream from the tank, could help to keep corals surface water. This will provide seawater at ambient tem-
clean. Further this also helps to eliminate the mucus perature and avoid potential contamination with microorgan-
layer they generate after the stress of the capture, isms from shallower depths untypical for CWC sites. Water
increasing remarkably the survival rate. Corals should collected by means of Niskin bottles can also be stored in a
not be fed during this initial period as they will gener- dark cool room for some days to replace the water from the
ally not eat (polyps are frequently retracted during the tanks if necessary. This is recommended if weather condi-
first days) and food decomposition may negatively tions or stays at harbours do not allow collection of seawater
affect water quality. From our experience, clean water on a regular basis.
and high current flow are more relevant for maintaining Under situations where ideal storage devices and equip-
coral viability than abundant food. ment are unavailable (tank, seawater flow, aeration system),
the collection and maintenance of living corals can be best
safeguarded by keeping corals in a bucket filled with cooled
seawater, ensuring frequent water substitution to provide
To ensure maximal survival rates and the best physiologi- oxygenation and storing if possible in darkness until trans-
cal condition, corals should be preferentially collected with port and transfer to the selected aquarium can be arranged.
video-assisted technology (ROV, manned submersible) to The aquarists from the Aquarium Finisterrae (A Coruña,
minimise damage during collection. After the experience Spain), who frequently collect deep-sea organisms (includ-
from M. Carreiro-Silva and her team from IMAR (Azores), ing corals) for exhibition and experimental purposes, use a
the use of a thermo-insulated bio-box installed in the ROV 300 L tank to keep animals alive, if space is available on
with close-fitting lid is particularly recommended for corals board the collection vessel. They place coral fragments in
collected at greater depths. The bio-box allows the storage of plastic grid boxes inside the tank to avoid samples moving
corals with deep-sea water, minimising exposure to tempera- out of place and getting hit during transportation. The tank is
ture fluctuations during ascendance to the surface. To further covered with a lid and kept under constant water inflow
minimise the risk of mortality, it is fundamental that coral (open circuit) until it arrives to land. The specimens from
colonies are quickly transferred from the stressing deck con- deep areas (800–1200 m depth) are immediately put into an
ditions to an environment that mimics as much as possible isothermal 400 L tank with a watertight cover and equipped
their original ambient situation; in practice this is primarily with a chiller unit that maintains water temperature at a level
accomplished by placing the corals in a cold seawater tank in similar to their natural habitat. This tank also has mechani-
darkness. On the open ocean seabed, CWCs typically occur cal, biological and chemical filtration as well as a protein
in environments with temperatures ranging from 4 to 8 °C fractionator, an ultraviolet (UV) unit and a recirculating
(although summer temperature can reach 12 °C off Norway pump that generates water currents inside the tank (Fig. 38.1).
or in the Gulf of Mexico), depending on location. In the deep This system is very convenient for expeditions that take sev-
Mediterranean Sea, temperature is about 12 °C with little eral days, as it allows holding CWC in a closed circuit for
deviation from this figure (e.g. maximal temperatures of 10–15 days.
should be aware of the type of material to be received and

the time of arrival. It is the responsibility of the host aquaria
to adjust the system settings in advance (aerators, filters,
proper seawater temperature, and light level) to guarantee
the wellness of the corals. A few days of acclimation are
optimal to progressively reduce the level of stress. To
achieve acclimation it is important to monitor polyp activity
and tissue condition several times per day. Stress signs
include closed polyps, and tissue sloughing and loss, as well
as extensive mucus production. Assessing tissue condition
is relatively easy in corals with coloured tissue, as it is the
case for the yellow Dendrophyllia cornigera, but in the case
of the white corals, the degree of polyp opening should be
used as a “control” of coral condition instead. Different
methodologies can be applied to help in reducing the signs
of stress and achieve acclimation, depending on which are
the feasible logistics. If ambient seawater is available, a
slow mix of this water and the water of the home aquaria is
a good strategy to facilitate coral acclimation. Current speed
should also be tested and optimised to achieve polyp exten-
sion, as this is frequently one of the most important aspects
for successfully keeping corals in a good shape. From our
experience, feeding should be restricted during the first days
following transfer, however after a couple of days, the addi-
Fig. 38.1 The isothermal tank used by the Aquarium Finisterrae to tion of liquid food close to the polyps can stimulate their
keep deep-sea fauna alive at sea. The tank is located on the top of the so extension, probably as a result of stimulus on coral’s chemi-
called “vital support” system which contains a skimmer and mechani-
cal, chemical and biological filters (all of them placed in the black box). cal receptors. Once the polyps are open it is also easier to
Behind the isothermal tank (not visible in the photograph) are located check which is the current speed they prefer. In the specific
the ultraviolet unit as well as the chiller. (Photo: © A. Veiga) case of Mediterranean CWCs collected for tank experi-
ments, various Lophelia pertusa and D. cornigera collected
The following steps concern sample transportation to the in 2006 and 2008 are still alive and in healthy conditions in
scientific aquaria facilities and coral transfer and acclimation the aquaria facilities of the ICM-CSIC (Barcelona, Spain)
into the aquaria. These operations are also highly critical for and the CSM (Monaco) respectively.
the viability of corals. Corals need to be transferred from the
ship to a vehicle while keeping them refrigerated. A fully
equipped cooled vehicle is the best solution for such pur- 38.2.2 Short Term Experiments on Board
pose. Alternatively, electric or cool boxes, portable
refrigerators and/or thermal bags may be adequate. Careful Fully equipped research vessels may provide opportunities to
planning of appropriate paperwork may also be required. It is conduct short-term experiments with live CWCs on board
necessary to be aware of the protection status of many CWC (e.g. Maier et al. 2006, 2007; Taviani et al. 2011; Hennige
species, as for instance all scleractinian and antipatharian et al. 2014; Orejas et al. 2017). Such practice presents advan-
corals are included in CITES Appendix II (https://www. tages and disadvantages. Advantages include: (1) measuring
cites.org) and many are protected under different regulations physiological functions very shortly after sampling using
(in the case of the Mediterranean Sea, it is necessary to check freshly collected specimens that might be more closely mim-
the Barcelona Convention: http://web.unep.org/unepmap/ ). icking the response of in situ conditions than specimens
Another important aspect to consider is to ensure that maintained over long periods under more artificial aquarium
the requirements set forth by port authorities are met in conditions; (2) the possibility to use seawater from the coral
order to get the official clearance to leave the harbour. collection point, instead of artificial seawater or water from
Living corals may also be transported by other means than shallow areas. Indeed, obtaining clean seawater can be expen-
land vehicles, such as ships or aeroplanes. It should how- sive and time consuming, and coastal water does not always
ever be kept in mind that not all air companies allow the mimic conditions found near CWC habitats. This is particu-
transport of living corals. larly true if corals are maintained in a region different from
The final destination for collected corals is often a scien- where they were collected; for example, the chemistry of the
tific laboratory or exhibition aquarium. These host aquaria Pacific and Atlantic oceans differs greatly. Disadvantages
include: (1) short acclimation time even in long cruises; iour and physiological response of CWC to the predicted
(2) the response of the organisms is only “short term” and effects of global climate change (global warming and OA).
need to be considered with caution. Some species are tolerant Results of these experiments are reported in Hennige et al.
to sub-optimal conditions, thus experiments conducted under (2014, 2015).
these conditions should be interpreted with caution. This is Another example of short-term experiment on board is a
especially the case if corals have been living in aquaria for study conducted by A. Gori and C. Orejas (unpublished data)
extended periods (e.g. years), since its unknown if aquaria in 2015 during the ANNA cruise on board the German RV
conditions can modify basic aspects of the physiology of Meteor off Angola, a location where the CWC L. pertusa
CWCs, related to changes in feeding regimes and chemical builds impressive reefs under very low oxygen (O2) concen-
properties of seawater. Therefore both short- and long-term trations. They conducted a physiological experiment on board
experiments encompass limitations with respect to the inter- aimed at analysing the physiological response under the natu-
pretation of a CWC response to measured variables for differ- ral low O2 conditions (2 mL L−1) and saturated O2 conditions
ent reasons which should be kept in mind when evaluating ex by measuring respiration, ammonium excretion and calcifica-
situ experiments in general. tion rates of the corals. The experimental set-up on board con-
In the following paragraphs some selected examples of sisted of incubation chambers (~400 mL volume), which
short-term experiments conducted on board research vessels were filled with water collected close to the seafloor using
are presented. Niskin bottles. Each experimental chamber included a stirrer
In 2012, S. Hennige from the University of Edinburgh and to keep the water in movement; once filled, chambers were
his co-workers conducted short-term ocean acidification closed with a lid and sealed with parafilm to avoid any gas
(OA) experiments under different temperature regimes, on exchange. During the entire experiment water renewal was
freshly collected L. pertusa samples on board of the Bristish manually carried out every 6 h in order to provide the corals
RRS Discovery (Hennige et al. 2014). Corals were main- with fresh seawater and to avoid an ammonium increase in
tained on board in experimental ‘coral hotels’, which are the chambers. Temperature and O2 concentration were care-
self-contained 430 L units containing ~350 L of seawater, fully controlled in every chamber before each water renewal.
with built in water circulation pumps, filtration units and Figure 38.3 displays the experimental set-up on board of the
chillers (Fig. 38.2). RV Meteor. No differences were observed in the respiration
Water circulation in these closed systems was ~300 L h−1. rates between corals maintained under natural low O2 and
To alter the carbonate chemistry in the experimental tank, increased O2 conditions, whereas respiration significantly
pre-mixed (e.g. with mass flow controllers) or purchased increased during the week of incubation.
gases with elevated CO2 were bubbled continuously into the From 2005–2008 cruises to the North Atlantic and
water. To reduce the change in pH following water changes, Skagerrak took place on the Dutch RV Pelagia equipped
freshly collected seawater was pre-bubbled prior to addition with a cool- and a radioisotope container for on board experi-
to the tanks. Subsequently, 30% of the seawater in the tanks mentation with CWCs and deep-sea sponges (van Duyl and
was exchanged every 2 days following feeding to ensure Duineveld 2005; Maier et al. 2006, 2007). This allowed the
build-up of detritus to be minimal. This kind of experimen- study of nutrient dynamics and the role of prokaryotes on
tal set-up contributed to get insight on the short-term behav- CWC ecosystems using freshly collected specimen of L. per-
Fig. 38.2 “Coral hotels”

used at SAMS to keep the
corals alive. The compartment
in the right contains the
chiller and electronic devices
and the compartment in the
left is filled with sea water to
host the corals. (Photo: ©
A. Gori)
Fig. 38.3 Maintenance and

experimental set-up for CWC
on board RV Meteor. a) Two
chillers are connected to two
tanks (acclimation and
experimental) to maintain a
constant temperature, b)
experimental set-up with
control and experimental jars
(containing Lophelia pertusa
nubbins) to measure
respiration and calcification
rates. The water is kept in
motion by the shaking plate
underneath the jars and the
stirrers inside the jars.
(Photos: © A. Gori)
Fig. 38.4 Sampling of CWC during cruises in the North Atlantic and board, (b) ambient bottom water used for on board experiments was
Skagerrak. (a) Sampling of CWCs using a box corer with a lid. The box sampled using a 1000 L water box, (c) Lophelia pertusa nubbins
corer was sealed with bottom substrate avoiding contamination of bot- mounted in methacrylat bases to conduct the experiments on board.
tom seawater with shallower water when hauling the box core back on (Photos: © C. Maier)
tusa and Madrepora oculata (Fig. 38.4; Maier et al. 2011, there are published in situ growth rates measurements for
unpublished data; Weinbauer et al. 2012) or sponges (van L. pertusa and M. oculata from the Mediterranean (Lartaud
Duyl et al. 2008). During the cruises in 2007 and 2008, addi- et al. 2013, 2014, 2017a, b, this volume) as well as for L.
tional radiotracer studies were conducted using 45-calcium pertusa from the Gulf of Mexico (Brooke and Young 2009).
to measure skeletal growth of L. pertusa from two sites Results indicate comparable growth rates for in situ and ex
(Mingulay and Skagerrak) and to conduct a first test on the situ measurements for old polyps of both species and faster
effects of OA on CWCs (Maier et al. 2009). As the calcifica- growth rates for young polyps of L. pertusa in the
tion rates obtained during these first onboard experiments Mediterranean (Lartaud et al. 2013). In contrast, for L. per-
appeared realistic (unfortunately no comparative in situ data tusa from the Gulf of Mexico, growth rates comparable to
were available at that time, but see new recent data in Lartaud those in the lower range obtained in aquaria, have been docu-
et al., this volume and references therein), the approach of on mented (Brooke and Young 2009).
board experimentation was continued during two projects To minimise stress during CWC collection, a special sam-
(MECCA and COMP) to study the calcification of pling device was designed by the COMEX engineers. This
Mediterranean CWCs under the lead of the Marine Protected device is a miniature copy of the “Croix St. André” formerly
Areas Agency (AAMP) on board the French RV Minibex used to sample the precious red coral Corallium rubrum
(COMEX), as well as during the MEDCOR cruise 2009 on (Fig. 38.5a, b). The device is an extremely efficient and less
board the Italian RV Urania (Maier et al. 2012). Currently destructive sampling tool reducing fragmentation of coral
Fig. 38.5 Sampling and on board experiments during Minibex cruises (b). On board maintenance and experiments were conducted in a single
in the Mediterranean. a) The ancient sampling gear “Croix St. André” container equipped with chilling unit, circulation pumps and a filtration
was the inspiration to construct a miniature version to more efficiently unit consisting of two micron bags with 5 and 1 μm mesh size (c, d).
sample small CWC colonies with the ROV that was dropped together (Photos: © C. Maier)
with the colony entangled in the mesh ends into the buckets on the ROV
branches that may otherwise lost in the soft sediment under- budget can be determined from a single incubation (Maier
neath. On board, the experimental set-up was kept simple et al. 2016).
using either open (aerated) or closed incubation containers
that were kept in the CWC storage container at 13 °C. In
closed system incubations, the seawater chemistry can 38.3 C
old-Water Coral Aquaria Facilities
change significantly as a result of coral metabolism, chamber in Research Institutes, Universities
volume and time of incubation (Maier et al. 2009, 2012). and Public Aquaria
Despite the changes in carbonate chemistry, calcification
rates derived from closed system incubations proved to be This section intends to offer an overview of some of the
comparable to open system incubations (Maier et al. 2012) aquaria facilities currently available in different research
and were comparable to those obtained in long-term aquar- institutes, mostly in European laboratories but also from
ium experiments (Maier et al. 2013b) and in situ measure- the USA. Even though this book focuses on Mediterranean
ments (Lartaud et al. 2014, 2017a, b). Closed system CWCs, we considered that in such a recent field of research
incubations are easier (and frequently the only ones) to use as the maintenance and experimental work with CWCs,
on board and might therefore facilitate large scale inter- any experience in the husbandry of CWCs will be of great
regional comparisons of CWC calcification growing under use to all researchers (Box 38.2). The facilities of 9
different environmental conditions with respect to tempera- research institutions are presented here as examples of
ture, salinity and carbonate chemistry. Another advantage of possible approaches which may be employed, and at the
closed system incubations is that both calcification and res- end of the chapter we include a list with some of the
piration can be determined in parallel and together with the aquaria infrastructures for CWCs we have been able to
determination of other parameters (dissolved inorganic car- identify. We hope we will be able to update this list in
bon, total organic carbon) the CWC carbon (C) and energy future editions of this volume.
Box 38.2: Best Practices on Basic System Requirements that maximise the growth potential of the naturally
The choice of the most adequate aquaria system to occurring nitrifying bacteria. The type or size
keep CWCs depends on the proximity to the sea, and should be according to the expected maximum bio-
the amount of money available for system set-up and load and waste.
maintenance. The best aquarium design is an open –– Mechanical filtration serves mainly to collect parti-
water system with a continuous intake of seawater. cles that may be found in suspension in the water
Ideally, seawater should come from the deep to mini- (organic and / or inorganic), protecting gears and
mise differences in water quality parameters between parts from physical damage or clogging (e.g. sand
the aquaria and natural habitat. However, setting up a getting into pumps) and collecting organic matter
deep-sea water intake is expensive, and if salinity of a before it decomposes. But since we are working
shallow water source does not vary a lot, this is also a with filter feeding organisms, this also interferes
good alternative. Having a constant water supply has with / compromises the availability of food.
the advantage of easy removal of waste, avoiding the –– Chemical filtration, comprises not only the non-
build-up of toxic nutrient levels, and continuous biological removal of dissolved substances from the
replenishment of oxygen and consumed minerals (e.g. aquarium (such as using activated carbon), but also
calcium). Closed system can be efficient too, but are other methods such as foam fractioning (or protein
more expensive and technologically complex, requir- skimming), ozonation and ultraviolet sterilisation.
ing an elaborate filtration system. Although none of these is absolutely necessary, all
of them can be very helpful in the export or mitiga-
–– Aquaria systems should ideally be mounted inside a tion of unwanted inorganic / organic material from
temperature controlled room to avoid large temper- the aquaria.
ature variations in the aquaria. Aquaria systems –– For open system aquaria the water quality is mostly
may vary depending on their use (i.e. exhibition or ensured by a proper water renewal (new water
experimentation) but should include stock / quaran- inflow). So, assuming a source of good water qual-
tine aquaria of at least 50 L capacity in addition to ity, the filtration system main focus should be on
the systems for the actual experiments / research. eliminating or mitigating possible inflow of harmful
–– Aquaria and their shelves should be as versatile as elements. This mainly includes mechanical filtration
possible so this will not limit future experimental of inorganic suspended sediments, and / or organic
designs. There are several options for the aquaria matter or unwanted and possibly harmful living
building materials, depending on the budget, the organism that may be coming along with the new
purpose, durability and on maintenance require- water. Another approach to mitigate the possible
ments. For example, glass is stronger and cheaper, inlet of living organisms may be chemical filtration,
but also breakable and heavier than plexiglas such as ozonation or ultraviolet sterilisation of the
(acrylic) or polycarbonates, but on the other hand incoming water, thus disabling or even killing them.
some of these plastics might get slightly opaque or –– Evaluation of the ideal seawater renewal rate or in
easily scratched with time. flow rate depends on the type of system (open or
–– Seawater refrigeration units should be slightly over closed), type of filtration system, and number of
dimensioned, considering expected maximum corals in relation to volume of water in each aquar-
water renewal / turnover / in flow rate, and they ium. All these factors will influence nutrients and
should be independent to each separate aquaria sys- waste build-up and thus water quality in aquaria.
tem mitigating possible damage / losses from one of Generally it can be considered good practice to
the units breaking down. replace 10–50% of seawater weekly or monthly
–– For closed aquaria systems the main focus of a from each aquarium using properly matured
basic filtration system is on the water quality in bio-filters.
terms of nutrients / organic waste, and similarly to –– The type of submersible recirculation pumps
most common seawater aquariums, it should cover (stream or pulsating), direction (laminar or turbu-
first of all the biological filtration, but also mechani- lent) and current velocity depend on the coral being
cal and chemical filtration. maintained (see Sect. 38.4)
–– Biological filtration converts the waste products to a –– The control / monitoring of parameters usually
less to non-toxic state. This is mainly attained by comprise inorganic nutrients (e.g. ammonia, nitrite,
various types of bio-filter systems and materials nitrate and phosphates), pH, temperature, salinity
(continued)
The aquaria facilities include several tanks (Fig. 38.6)

Box 38.2 (continued) installed in thermo-regulated rooms allowing mimicking deep-
and total alkalinity (especially for closed systems). sea temperatures. The cool-rooms are supplied with natural
Depending on the experimental design, and objec- seawater pumped from 10 m depth. Once the water is trans-
tives of the study, some other parameters might ported into the cool-room, a storage tank is filled and tempera-
require monitoring. ture is regulated to reach the 13 °C by means of a chiller before
–– Lights should be kept off whenever possible, recre- filtration by a 5 μm mesh size filtered and after this distributed
ating the coral’s natural environmental conditions. to the different aquaria. Water is continuously distributed to
The use of red filters on the lights (or red light bulbs) allow a complete water renewal from 1 to 4 times per day in
may help reduce possible impacts by the necessary each tank over 80 L tanks or 50 L recirculating flumes (Purser
light exposure. In addition, this also helps to avoid et al. 2010), depending on the experimental requirements.
unwanted algae proliferations in the aquaria. Corals were maintained in the dark, fed three times a week with
–– Electrical installation / wiring and plugs should be live Artemia nauplii, and the environmental conditions (tem-
above water level with some safety distance to min- perature, pH, conductivity, oxygen saturation) are continuously
imise the chances of getting water splashed and monitored. Safety equipment is installed to prevent any prob-
waterproof parts should be installed whenever pos- lems (water-level sensor, seawater cut-off, temperature anoma-
sible. Extra plugs should be available, for lab equip- lies, etc.). This experimental design was developed for medium
ment. Each aquaria system should have individual (months) to long-term (years) experiments.
sets of electrical wiring / switches to ensure that an The experiments conducted in the Banyuls-sur-Mer infra-
electrical problem on one system does not compro- structures address questions regarding CWC response to
mise the others. environmental changes and anthropogenic threats, the first
one in order to forecast the response of Mediterranean CWCs
to current and future environmental conditions predicted by
the IPCC. Integrative studies are executed at distinct physi-
38.3.1 Aquaria Facilities for Cold-Water Coral ological levels including skeleton growth, energy acquisition
Maintenance at the Benthic and coral associated bacterial communities (Lartaud et al.
Ecogeochemistry Laboratory (LECOB) 2013, 2014; Meistertzheim et al. 2016). Conducted experi-
of Banyuls-sur-Mer, France ments aimed at investigate the resilience of reef-building
CWCs and their function in canyon ecosystems, particularly
The LECOB laboratory at Banyuls-sur-mer marine station regarding the effects of potential changes in temperature,
(Oceanographical Observatory, Pierre and Marie Curie current speed, and organic matter concentrations.
University) has been equipped with aquaria facilities for cold-
water scleractinian and gorgonian corals since 2010. The labo-
ratory is located on the West coast of the Gulf of Lions, in the 38.3.2 Cold-Water Coral Maintenance Facilities
Mediterranean Sea. This area is close to the Lacaze-Duthiers at the Centre Scientifique de Monaco
submarine canyon (canyon head is 23 km off Banyuls-sur- (CSM) (Principality of Monaco)
Mer), where L. pertusa and M. oculata frameworks occur,
together with Desmophyllum dianthus and Dendrophyllia cor- The CSM has 10 years’ experience in maintaining CWC spe-
nigera corals. This canyon and the coral ecosystems are part of cies; specifically, L. pertusa, M. oculata, D. cornigera,
the Gulf of Lions Marine Nature Park MPA. Dendrophyllia ramea and D. dianthus sampled in deep waters
Fig. 38.6 Aquaria facilities in the Marine Laboratory of Banyuls-sur-Mer, France. (Photo: © E. Peru, LECOB)
Fig. 38.7 Coral fragments of

Dendrophyllia ramea (pink/
orange coral) and
(yellow coral) in the small
30 L aquaria in the aquaria
facilities of the CSM. (Photo:
© S. Reynaud)
of the Mediterranean Sea, have been maintained in the CSM pumped to the 28 aquaria. Continuous water movement
aquaria infrastructures. Currently, specimens of D. cornigera inside each aquarium is provided by submersible pumps with
and D. ramea have been grown in the CSM aquaria for more a flow rate of 10,000 L h−1 in the large maintenance aquaria
than 6 and 2 years, respectively (Fig. 38.7). The corals are and 2000 L h−1 in the small experimental aquaria. Moreover,
maintained in the dark, either in large 100 L aquaria for genin the large maintenance aquaria, flow intensity can be regu-
eral maintenance (at 12 °C), or in 30 L aquaria for experimen- lated and wave action simulated. As a security measure, in
tal purposes (at different temperatures). Seawater renewal is case of malfunctioning of the seawater cooling system, the
provided by a continuous flow of Mediterranean seawater pumping of water from the storage tank is automatically
pumped from 50 m depth at a rate of 1 m3 h−1 and pre-cooled blocked when seawater temperature exceeds 15 °C. In that
at 11 °C. Water temperature is then slightly heated to 12 °C or case, corals are maintained at 12–14 °C in their aquaria by
more using 300 W heaters connected to temperature control- the air temperature controlled chamber. Currently, the
lers, or cooled down to lower temperatures using chillers. aquaria harbour scleractinian CWCs, as well as gorgonians,
Submersible pumps with a flow rate of 400 L h−1 provide con- black and soft corals and sea pens.
tinuous water movement inside each aquarium. Corals are fed
4 times a week with frozen Mysis (Crustacea, Eumalacostraca).
38.3.4 The “DeepSeaLab”, Instituto do Mar
(IMAR), University of the Azores in Faial
38.3.3 Cold-Water Coral Maintenance Facilities Island (Azores, Portugal)
at the Institut de Ciències del Mar
(ICM-CSIC) (Barcelona, Spain) The DeepSeaLab at IMAR, University of the Azores on Faial
Island is an aquaria facility dedicated to research with deep-
Cold-water corals have been maintained at Institut de sea organisms, conceived and designed in collaboration with
Ciències del Mar (ICM-CSIC) since 2006 in an updated ver- the Oceanário de Lisboa in 2009 and subsequently renewed
sion of the system developed by Olariaga et al. (2009). The and enlarged in 2015. The aquaria facility is composed of 5
aquaria are located in a 15 m2 temperature-controlled experi- independent aquaria systems set-up in a temperature-
mental chamber in the “Area of Experimental Aquaria” controlled room at 14 °C in darkness. One semi-closed water
(ZAE) of the ICM-CSIC. Air temperature inside the cham- system is used for the maintenance of corals and other deep-
ber is maintained between 12 ºC and 14 ºC in complete dark- sea organisms that are not being used in experiments, and
ness conditions. Corals are kept in four 140 L maintenance four open-water systems used for the experimentation
aquaria (Fig. 38.8) and twenty-four 25 L experimental (Fig. 38.9). The existence of a semi-closed water system
aquaria. Seawater is provided by a continuous flow of ensures that in the case of seawater supply failure, corals can
Mediterranean seawater directly collected in front of the still be maintained in a fully closed system. All systems are
institute facilities and pumped from a depth of 15 m at a equipped with a water temperature controller. The tempera-
maximal inflow capacity of 300 L h−1, then filtered with a ture sensors have 1 °C accuracy and a minimal hysteresis of
50 μm pore size mesh and cooled at 12 °C. Seawater enters 1 °C. The water supply to the aquarium systems is continu-
the chamber directly to a 120 L storage tank, from where it is ously pumped from coastal waters (5 m depth, salinity: 36).
Fig. 38.8 Overview of the

CWC aquaria facilities at
ICM-CSIC in Barcelona.
(Photo: © S. Ambroso)
Fig. 38.9 (a) Aquaria

infrastructures in the
DeepSeaLab, (b) detail of a
tank showing the water bath
to minimise fluctuations in
seawater temperature between
replicate experimental
aquaria. (Photos: © R. Sá da
Bandeira)
The water is stored in a 410 L storage tank equipped with a An example set-up used previously (Fig. 38.10) had 20
cooling unit and a thermostat. Water is filtered first through a independent closed-loop systems, each with an additional
50 um felt filter bag (FSI®) in the storage tank and through 4 experimental tanks (5 L each) for separation of biologi-
an additional 5 um felt filter bag in each experimental system cal material. Total volume of each system including the
as well as UV sterilised. Water is then pumped into sumps in sump is 80 L, and includes individual temperature control
the individual systems where it is cooled again and subse- and biological filtration. Gas mixing for OA experiments
quently distributed to the individual experimental aquaria. A is achieved in house using mixing flasks, and analysed
freshwater water bath equipped with a cooling unit ensures continuously with a Li-820 gas analyser (Licor). Ambient
that the water in individual experimental aquaria (e.g. repli- and elevated CO2 air mixes (e.g. at 750 and 1000 ppm) are
cate aquaria within the same experimental treatment) is con- plumbed around the room and into sump tanks to modify
stantly maintained, while maximising space for the water carbonate chemistry (Hennige et al. 2015; Gori
experiments. Each aquaria system has the capacity to inde- et al. 2016).
pendently manipulate temperature and pH (through a combi-
nation of CO2 bubbling and/or CO2 removal through a soda
lime filter) enabling the simulation of conditions predicted as 38.3.6 Aquaria Facilities of the University
consequences of climate change (Carreiro-Silva et al. 2014). of Gothenburg, Sweden (Sven Lovén
In addition, the facility is equipped with 100 L stock tanks Centre for Marine Infrastructure)
and dosing pumps for the delivery of sediments or food par-
ticles in different concentrations for feeding and deep-sea The marine station of the University of Gothenburg (UGOT)
mining experiments. Currently, the aquaria maintain cold- at Tjärnö offers excellent opportunities for both experimen-
water scleractinians, gorgonians, black corals, zoanthids and tal and field based research on L. pertusa. The station is situ-
anemones. ated on the Swedish west coast in the vicinity (~10 nautical
miles) of several shallow coastal L. pertusa reefs in the NE
Skagerrak. The Tisler reef is the largest of these reefs with
38.3.5 Cold-Water Coral Aquaria Facilities living coral extending over an area of ca. 250 ha at a depth of
of the “Changing Oceans Group” at the 70–145 m (Lundälv 2003). The facilities include several
University of Edinburgh (Edinburgh, constant temperature rooms with a flow-through system with
United Kingdom) seawater taken from 45 m depth in the Koster Fjord, adjacent
to the laboratory (Fig. 38.11). The fjord and surrounding
The Changing Oceans Group experimental mesocosm facility areas are fed with deep oceanic water from the Atlantic that
was rehoused and refurbished in 2017 to increase capacity and is funnelled via the Norwegian Trench allowing for simula-
flexibility for conducting CWC and OA experiments, with tion of deep-sea conditions in the laboratory. L. pertusa has
flexible racking and tank systems. Seawater can either be col- been successfully reared in these facilities since mid-2000’s
lected from the East coast of Scotland, or artificially made. (see Sect. 38.1).
Fig. 38.10 A previous set-up

of the Changing Oceans
Group experimental
mesocosm facility. (Photo: ©
S. Hennige)
Fig. 38.11 CWC aquaria

facilities at the marine station
of the University of
Gothenburg, Tjärnö, Sweden.
(Photo: © C. Orejas)
38.3.7 Cold-Water Corals Aquaria ies. To reduce the total alkalinity, the ASW is treated with
Facilities at Temple University strong acid (12.1N HCl) followed by a period of air bubbling
(Philadelphia, USA) to facilitate off gassing of excess CO2. This method has been
effective at producing seawater conditions that approximate
The aquarium system at Temple University in Philadelphia the natural environment of deep-water corals (Lunden et al.
was first established in 2009 using primarily hobbyist equip- 2013; Georgian et al. 2016b).
ment within a temperature-controlled room. In 2010, a sec- The latest efforts using these systems include mainte-
ond system was added within a standard laboratory room nance of octocoral species from the GoM. From personal
without temperature control, but including a temperature- observations, octocorals appear to be much more sensitive to
insulated “lobster tank” paired with an aquaculture-grade laboratory conditions than scleractinians corals, thus neces-
recirculating chiller. These two systems, while differing sitating careful management of water quality, feeding, and
slightly in their mechanism of temperature control, utilise flow. Thus far, efforts to sustain octocorals have been suc-
similar designs in terms of waste removal and water flow, cessful, aided by the use of improved artificial salts, wave
and each has continuously supported CWCs from September makers, power heads, regular water changes, and target feed-
2009 up until the present day. A detailed description of this ing with a variety of food sources.
system is available in Lunden et al. (2014a). In support of
ongoing research activities in the Gulf of Mexico (GoM), the
recirculating aquaria at Temple were designed primarily to 38.3.8 Aquaria Facilities in the Oregon
maintain scleractinian CWCs for global ocean change and Institute of Marine Biology
anthropogenic disturbance studies (e.g. Lunden et al. 2014b; (Oregon, USA)
Georgian et al. 2016a, b; Kurman et al. 2017). Now, these
aquaria house octocorals being used in further studies of OA, The aquaria system in Oregon was initially conceived at
and additional L. pertusa colonies for use in oil and disper- Harbor Branch Oceanographic Institution for studies on
sant exposure experiments. deep-sea echinoderms, and was subsequently used to main-
Other than all previous examples, Temple University uses tain Oculina varicosa. The system was housed in an insu-
artificial seawater (ASW) in its facility. In a recirculating sys- lated building and comprised four independent sets of five
tem at an institution far from the sea, this is a necessary and tanks, each with a chiller unit that could be programmed for
ongoing expenditure; however, ASW usage for water changes a specific temperature, and a recirculating pump. Since the
can be reduced by efficient filtration systems. The filtration facility was located at an estuary, water for the system was
system at Temple University includes a protein skimmer, live brought in from offshore and stored in a large (5678 L) recir-
rock, Jaubert plenum, and UV steriliser (Fig. 38.12). A sec- culating tank until needed. In 2001, this system was relo-
ondary consequence of utilising ASW is an additional need to cated to the Oregon Institute of Marine Biology, which is
modify the total alkalinity of the seawater, due to ASW’s high situated on the Pacific coast and therefore has ready access to
buffering capacity. This is particularly necessary for OA stud- natural seawater.
Fig. 38.12 Recirculating
aquaria at Temple University
for CWCs. Top right: holding
tank; top left: TECO
recirculating chiller; bottom:
sump tank with biological and
chemical filtration.
Reproduced from Fig. 1 of
Lunden et al. 2014a L&O:
Methods. (Photo: J. Lunden,
reproduction of the figure
authorised by Wiley. © Wiley)
Fig. 38.13 Schematic of a

single CWC maintenance
tank system operated at
Oregon Institute of Marine
Biology, showing the lateral
view. The different
components are labelled and
the water flow indicated by
arrows. The valves are used to
adjust water flow, and for
isolating individual tanks for
cleaning. (Scheme: © Sandra
Brooke)
Each tank series comprises five fibreglass rectangular the substrate. This arrangement also allowed for moving the
tanks (1.2 × 0.6 × 0.46 m; 330 L) that are positioned above a corals to a clean tank with minimal handling. The gravel
larger sump (1.8 × 1.2 × 0.75 m; 1600 L). Water is pumped served to maintain appropriate carbonate chemistry, captured
from the sump through a 0.5 horsepower self-priming pump, any waste organic material (which was then removed during
through a UV light steriliser and into a chiller. After chilling, cleaning) and provided a substrate for beneficial bacterial
the water is pumped into the tanks via a simple filter system, growth.
consisting of a household canister style sediment-filter that
removes particles >10 μm. Each tank has a feeder line with a
pressure disperser on the end to avoid a hard jet of water 38.3.9 Aquaria Facilities in the Aquarium
entering the tank. At the opposite end of the tank, the water Finisterrae (A Coruña, Spain)
leaves through a standpipe and empties into the sump. Valves
placed throughout the system are used to control the flow The public Aquarium Finisterrae has quarantine facilities
rate, and excess water is bypassed back into the sump as well as research tanks. The receipt of the CWC speci-
(Fig. 38.13). The bottoms of the CWC tanks were covered mens takes place in the quarantine area, where the newly
with a layer of aragonite gravel, and a piece of rigid plastic arrived organisms are acclimated to the aquarium water
square mesh (1 × 1 cm × 1 cm deep) was placed on top of the properties (Fig. 38.14a). Acclimation process is slow and
gravel to support the coral fragments and raise them above carefully avoiding abrupt changes in the physiochemical
Fig. 38.14 (a) Dendrophyllia

cornigera in a quarantine tank
of the Aquarium Finisterrae.
The holes on the base are
used to provisionally place
the colonies to avoid its
movement. (b) Specimens of
Veretillum cynomorium in an
exhibition tank of the
Aquarium Finisterrae. (Photo:
© A. Veiga)
water conditions (especially temperature, pH and dissolved

oxygen). The quarantine tanks used in the Aquarium 38.4 Cold-Water Coral Maintenance
Finisterrae for these animals can hold up to 1400 L, and
recirculating pumps are usually placed inside them (whose This section has been divided in several subsections to pres-
flow depends both on the volume of the tank and the type ent different experiences on the maintenance of different
of hosted animal). Corals are properly fixed in the aquaria CWC groups (Box 38.3). Maintenance of scleractinian cor-
to avoid the displacement of the specimens by the currents als, gorgonians, black corals and sea pens are presented here,
inside the tank. In case there is need of cold water input, a some correspond to Mediterranean infrastructures, some to
heat exchanger or a chiller unit can be used. Nevertheless, infrastructures located in other European countries or in the
the choice of the chilling system will depend on the vol- USA. A final subsection on coral nubbin preparations for
ume of the tank, of the desired final temperature, as well experimental purposes is also included.
as the temperature and the input rate of the renewal water.
In the acclimation tanks usually used in the Aquarium
Finisterrae, specimens of both L. pertusa and M. oculata 38.4.1 Maintenance of Scleractinians
were kept for several months in the quarantine zone until
they were moved to the exhibition aquaria, where they 38.4.1.1 A Mediterranean Experience: Long
were kept in similar conditions as the aforementioned. At Term Maintenance of four
the Aquarium Finisterrae several species of colonial Scleractinian Species
anthozoan have been maintained such as: some species of Four different species of hexacorals have been maintained
the genus Alcyonium, gorgonians like Leptogorgia sar- alive for more than a decade in the facilities of the Institut de
mentosa, or Eunicella verrucosa, sea pens such as Ciències del Mar (ICM-CSIC) in Barcelona. These species
Veretillum cynomorium (Fig. 38.14b), or the CWCs D. include Lophelia pertusa, Madrepora oculata, Dendrophyllia
cornigera, L. pertusa, and M. oculata, as well as the cornigera and Desmophyllum dianthus. All colonies have
anthipatarian Antipathella subpinnata. It is important to been kept in tanks with a capacity between 30 L and 150 L in
remark that most of these species also inhabit Medi running natural seawater, which is sequentially filtered (5 μm
terranean waters. and 50 μm mesh size), constantly renewed and kept in motion
The specimens collected for scientific research are placed using circulation pumps with a flow rate between 2000 and
in polycarbonate aquaria of 40 or 80 L, placed in a small 4000 L/h. Corals are generally glued onto labelled methacry-
isolated room that has its own water supply and an indepen- late holders using a two-component epoxy resin so they can
dent filtering system. This way, the studied material can be be kept in an upright position, although the type of support
subjected to different environmental conditions in a con- used can vary depending on coral size. Scleractinian colo-
trolled setting. The life support used in this installation has a nies are fed according to the size of their polyps. Colonies
chilling unit capable of keeping the circulating water at a bearing large polyps, such as D. cornigera (20–40 mm in
temperature of 10 ± 0.5 °C, a protein fractionator (“skim- diameter) and D. dianthus (15–30 mm in diameter), are gen-
mer”), a series of cartridge filters capable of filtering water erally given commercial frozen krill, Artemia salina or Mysis
up to 0.30 μm and an ultraviolet unit placed right before the relicta shrimps on a daily basis, which are directly supplied
tank’s water input. to each polyp using a plastic Pasteur pipette after they are
defrosted. It is important that the polyps are fully expanded

Box 38.3: Best Practices for Scleractinian CWC, before starting manual feeding. In general terms, colonies
Gorgonians and Black Corals Maintenance tend to extend their polyps daily if fed with regularity. If this
There is not a single magic recipe for coral mainte- is not the case, a solution composed of a wide range of food
nance, as depending on the species and its origin (e.g. particles (1–450 μm) can be diluted in the water tanks to
geographical region, current regime, depth, tempera- induce polyp expansion. Colonies bearing smaller polyps
ture) the optimum conditions will vary. However some (5–10 mm in diameter), such as M. oculata, are given com-
general aspects have to be taking into account for a mercial frozen Cyclops alternated with nauplii of live A.
successful CWCs maintenance. salina, which are homogeneously distributed in the water
tanks for the polyps to actively capture the prey. No issues
–– Temperature should be in the range of the area have been encountered with mixing different species of
where the corals were collected and kept as con- scleractinian corals in the same aquaria. However, a mini-
stant as possible (Box 38.1) mum distance between colonies is required to avoid any pos-
–– Flow through systems are highly recommended as sible contact between polyps when in full expansion.
they provide continuous clean water (Box 38.1) Occasionally, it has been observed that foraminifera may
–– Water chemistry should be checked daily (ammo- attach to the surface of L. pertusa and M. oculata nubbins. If
nium and nitrates should be kept at minimum lev- foraminifera are not manually removed, sediment and par-
els) (Box 38.1) ticulate matter tend to accumulate in the surface of the colo-
–– Tanks should have at least 50-75 L volume. Tank nies and the coenenchyme, which could lead to the death of
size depend on the number of nubbins / coral frag- the tissue and even to the whole colony.
ments per tank
–– Different CWC species can share a tank, but enough 38.4.1.2 Atlantic and Pacific Experiences: Long
distance between nubbins / fragments should be Term Maintenance of Lophelia pertusa
allowed in order to avoid any contact among the and Oculina varicosa
polyps Successful maintenance of scleractinians in aquaria
–– Scleractinians need high flow rates. A flow rate demands not only for proper water chemistry to be met, but
from 2000 to 4000 L/h is recommended also sufficient water movement. The rule, drawn from long
–– Feeding can take place daily, every two days or experience with L. pertusa, seems to be that the turbulence
twice a week. should be just below the limit for the polyp’s ability to man-
–– Food size and type have to be adapted to the polyp age (and thus be able to feed): that is, there should be a
size of the species: Generally frozen krill, Artemia noticeable strong flutter of the tentacles due to turbulence,
salina and Mysis relicta are suitable for Desmo but not so high that the polyp is prevented from positioning
phyllum dianthus and Dendrophyllia cornigera it’s tentacles to catch food. If the tentacles flop around fully
whereas copepods (Cyclops sp.) and Artemia at the mercy of the water movement, turbulence is too
salina nauplii are more adequate for Madrepora strong. The preferred system used for maintaining water
oculata, gorgonians and certain black coral spe- movement at the University of Gothenburg (UGOT) has
cies (Antipathes dichotoma). Lophelia pertusa can been the ‘Mississippi’ chambers; These are experimental
be fed with Artemia naupli, Mysis sp.,and also, chambers of 12 L volume within which a flow-through sys-
when available with calanoid copepods. Rotifers tem can be maintained to provide corals with an appropriate
are an appropriate food source for species with water supply, with paddlewheels integrated into the tank, to
very small polyp size such us the black corals mechanically maintain turbulence within the tank, whilst
Bathypathes sp. and Leiopathes glaberrima. not simultaneously creating bubbles, following an in situ
–– Prior to feeding the corals polyps have to be open. design first described in Tengberg et al. (2003). These pad-
If possible manual feeding (using a pipette, syringe dles, reminiscent of those used on historic Mississippi river-
etc.) is recommended. If polyps are closed chemical boats, consist of a long axle and 8 or more flat panels running
stimulation might be necessary, and can be achieved the length of the axis. By rotating the axis, the paddles rotate
by preparing a “soup” mixing different food types in the same direction, with the paddles each displacing
and releasing it in the aquaria. water in the same direction in turn; driving the riverboats on
–– After feeding, the remaining food must be removed. the Mississippi, or causing elongated displacement waves in
–– As CWC live in the aphotic zone, we recommend the Mississippi chambers. These Mississippi paddles are
maintaining the aquaria in darkness (Box 38.1). placed in the upper portion of the experimental tank, sepa-
rated by some cm from experimental coral nubbins. These
chambers differ from the initial Tengberg et al. (2003) set-up adding crushed krill to the water, which rapidly spread with
by facilitating chamber replication with a minimum of the circulating water through the entire aquarium. In
mechanical motors. The design of these tanks, and the asso- smaller aquaria, it was easier to perform controlled feeding,
ciated supply systems for dosing tanks continuously with and to remove food waste after the feeding. Based on this
various concentrations of food, pollutants etc. is presented experience, Mortensen considered that the most efficient
with a schematic drawing in Sects. 38.5.2 and 38.5.4. way of feeding the corals in a small aquarium was to turn
Although pumps could be used as well, it is important to off the water supply, and add food above the corals. The
make sure that no air bubbles are generated since these will food then slowly settles on the polyps. When the polyps
stress the corals and trigger mucus production and discharge have started ingesting the food, the water supply can be
of cnidae (stinging cells). The pump must also be mounted turned on again.
in a way that minimises vibrations. When using Mississippi- In the facilities from the Oregon Institute of Marine
type paddles it is important to mount the paddles in a way Biology, the CWC tanks were maintained at ambient tem-
that minimise surface splashing that also can produce air perature for the target species (16 °C for Oculina varicosa
bubbles and disturbances. The paddles are also a preferred and 8 °C for L. pertusa). The corals were fed every 3–4 days
option when corals are kept for breeding, since submerged using live A. salina nauplii, which were hatched from cysts
pumps would destroy the gametes. in a conical Artemia hatchery with seawater and an external
Keeping CWCs healthy in aquaria requires a sufficient light. Prior to feeding, the water flow was reduced to a rate
amount of high quality food, such as calanoid copepods, rich that maintained the appropriate temperature, but did not
in wax esters and lipids. The brine shrimp Artemia sp. is a flush the Artemia from the tanks. The corals were allowed to
common food item for corals in aquaria, since they are easily feed for 12–18 h every 4 days, after which time, a Nitex bag
reared and can be served alive. They are, however, probably (200 μm mesh) was placed over the standpipe outflow to
not sufficiently rich in nutrients (Larsson et al. 2013a) and it capture unconsumed nauplii, and the water flow was

is therefore recommended that they be fed with microalgae increased. Excess nauplii were removed to maintain low lev-
before feeding them to the corals. There are sources of frozen els of organic material and to prevent formation and accumu-
zooplankton, and at UGOT researchers have used Calanus lation of inorganic wastes, which is particularly important
sp., which is a common food source for L. pertusa in the for recirculating systems. This is a simple system with rudi-
North Atlantic (Dodds et al. 2009). Intact frozen copepods mentary water quality control, so in order to maintain healthy
have a tendency to float, and therefore the copepods have animals, every month a 50% water replacement was per-
been homogenised in a blender before feeding. Lipid droplets formed, and a complete system cleaning was done at least
and carotenoids from the copepods have been observed in every 6 months or more frequently if necessary.
histological preparations of mesenterial filaments of recently For long term maintenance, flow-through systems are
fed corals (Strömberg and Östman 2016), indicating that they ideal, but not always possible. A series of flow through
have indeed been feeding on the copepod suspensions. aquaria have been constructed at the Trondheim Biological
At UGOT, food is administered twice a week. Too fre- Station in Norway (by J. Järnegren, NINA) that are fed by
quent feeding can lead to accumulation of degrading food sand-filtered water drawn from 100 m in the Trondheim
residues and build-up of biodegrading bacteria and protozo- Fjord. A flow-through system is also available at the UGOT
ans that can harm the corals, as well as to elevated ammonia facilities at Tjärnö, Sweden. This system provides a continu-
and nitrate concentrations, both also harmful for corals. Even ous flow of ‘ambient’ water to the corals, and has proven
though corals potentially can use particulate organic material successful for long-term maintenance and research on early
as a food source, sediment inflow into the aquaria should be life history studies of L. pertusa (see Larsson et al. 2014;
minimised to avoid bacterial build-up. Also, the sediments Järnegren et al. 2017).
potentially bring other pathogens, such as protozoan para- It is also worth mentioning the DyMiCo, active sand bed
sites or bioeroding organisms. At UGOT researchers use 50- filter used by R. Osinga and collaborators in the University
and 5-micron Ametek polypropylene filter cartridges of Wageningen (The Netherlands). This filter was specifi-
mounted in sequence to filter the incoming water. This sys- cally designed to allow maximal plankton feeding while still
tem can require frequent filter changes depending on the having a very high water quality. The system is low mainte-
sediment concentration of the incoming water. A sand filter nance and works quite well for sponges and corals. Dr.
that is easily back-flushed could probably do the job with Osinga and his team currently have two 3000 L systems for
less maintenance and at lower cost. work on boreal deep water sponges. Both systems consist of
One of the problems when keeping L. pertusa in a large a water storage tank, a DyMiCo filter and 12 replicate 30 L
aquarium is to perform an efficient feeding of the polyps tanks for experimenting, in which temperature and pH can be
without altering the water quality due to decaying of accu- controlled individually. This facility is run currently at 6 °C
mulated food waste. Mortensen (2001) fed the polyps by in a climate controlled room.
38.4.2 Maintenance of Octocorals Apart from adequate flow conditions, gorgonians maintained
(Gorgonians, Soft Corals and Sea Pens) in the Azores appear to be quite voracious requiring abundant
and frequent feeding. They are fed every day twice a day (20 mL
In the aquaria facilities of Institut de Ciències del Mar (ICM- of food / 30 L aquaria) with a mixture of frozen A. salina adults
CSIC) in Barcelona, several gorgonian species and nauplii, mysids, microplakton, and a food supplement com-
(Acanthogorgia hirsuta, Eunicella singularis, Eunicella cav- posed of proteins, aminoacids, lipids, vitamins, and oligoele-
olini, Ellisella paraplexauroides, Paramuricea macrospina, ments (Marine Active Supplement, Bentos Nutrition) all partially
P. clavata, and Spinimuricea klavereni) and soft coral blended with a food processor. Feeding is supplemented with
(Alcyonium palmatum, Nidalia studeri and Paralcyonium live rotifers (Branchionus sp.) and microalgae (Chaetoceros sp.
spinulosum) of the Mediterranean continental shelf and slope and Nannochloropsis gaditana) five times a week.
have been successfully maintained for several years. At ICM-CSIC, most octocoral species are fed with com-
Acclimation of some of these species to aquarium conditions mercially frozen cyclops 3 days a week two times per day.
can be challenging. After placing colonies in different However, it has been observed that this diet is not suitable for
aquaria, polyps of some of these species remained con- A. hirsuta, as colonies progressively loose polyps and color-
tracted. However, it has been observed that if colonies are ation changes from bright orange to pale grey. After feeding
placed in large aquaria (over 150 L) equipped with submers- live nauplii of A.salina enriched with fatty acids and phyto-
ible pumps that can generate a flow rate of 4000 L h-1, polyps plankton (Tetraselmis sp.) to A. hirsuta for several months,
tend to extend more frequently and acclimation occurs faster. its original coloration was restored and polyp loss stopped.
The acclimation period may differ between species, lasting Occasionally, researchers from ICM-CSIC have observed
less than a week for some of them (e.g. E. cavolini and P. that some nubbins, especially of E. cavolini and E. paraplex-
macrospina), but can last up to several months in others (e.g. auroides, can be plagued by isopods, which can be removed
E. paraplexauroides). by submerging the nubbins for 5 s in a brackish solution of
After acclimation, gorgonians are commonly fragmented 50% seawater and 50% distilled water.
into several nubbins for experimental purposes (see Sect.
38.4.4, Fig. 38.16). The coenenchyme at the basal end of the
nubbin is removed exposing a portion of the axis (1–2 cm). 38.4.3 Maintenance of Antipatharians
This denuded portion is covered with specific coral epoxy putty (Black Corals)
(Coralfix Superfast, Grotech) and the nubbins are attached to
an acrylic base. Another system, employed by the DeepSeaLab The species Antipathes dichotoma, Leiopathes glaberrima
in Azores, consists in the use of sponge pieces that have previ- and an unidentified species of the genus Bathypathes have
ously been sterilised in ethanol and rinsed in distilled water to been maintained in the aquaria facilities at the Institut de
cover the denude portion. It is extremely important not to cover Ciències del Mar (ICM-CSIC) in Barcelona during long peri-
healthy coenenchyme parts with the coral glue as it may rap- ods of time (two years for A. dichotoma and Bathypathes sp.
idly lead to necrosis of the adjacent tissue (more details in Sect. and six months for L. glaberrima). Colonies of these three
38.4.4). In the CWC infrastructures in Barcelona, nubbins of species are kept in a 30 L aquarium equipped with a submers-
species dwelling on hard substrates are maintained in 30 L ible pump with flow rates of 2000 L h-1 and with 50 μm fil-
aquaria equipped with submersible pumps with flow rates of tered running natural seawater. In these cases, colonies are
2000 L h-1. Also in Barcelona, nubbins and colonies of species not divided into nubbins. Because of the small dimensions of
dwelling in soft sediments, such as A. palmatum and S. kla- their polyps, finding appropriate food sources for antipathar-
vereni, are placed over a layer of fine sands (~15 cm in height) ians has been challenging. After unsuccessfully trying differ-
in aquaria of 150 L provided with submersible pumps with ent food regimes (cyclops, live nauplii of A. salina and red
flow rates of 4000 L h-1. plankton), it was observed that these organisms can capture
Recent experiences with the maintenance of gorgonians live rotifera. In order to supplement their diet, rotifera are
(e.g. Viminella flagellum, Dentomuricea aff. meteor, enriched with phytoplankton (Tetraselmis sp.) and yeast.
Callogorgia verticillata, Paracalypthrophora josephinae, Antipatharians are fed five times a week two times per day.
Acanthogorgia armata) in the DeepSeaLab in Azores The species Leiopathes sp. and Antipathella sp. are cur-
revealed that apart from flow speed, flow direction is very rently maintained at the DeepSeaLab in the Azores. Recent
important to keep these species alive. Initially, a single pump observations of the feeding behavior of these species suggest
with a single outflow tube was mounted in the aquaria and that they have strong nematocysts and capture food particles
the polyps remained closed for days. However, the installa- easily but take a long time to ingest food because of the slow
tion of a pipe with many holes helped to redistribute the flow movement of their tentacles. Based on these observations it
into a more uniform laminar way and the polyps opened is advisable to feed them frequently (at least twice a day)
completely and started feeding normally. with low amounts of food.
38.4.4 Coral Nubbin Preparation

for Experimental Purposes
Coral nubbins, the genetically identical replicates (ramets)

generated from a single coral genet, have been proposed as
preferred source material for biological and molecular stud-
ies. The advantages to work with nubbins are several: sizes
can be chosen by the researcher depending on the aquaria
and experimental chambers used for different kind of mea-
sures to be carried out, further they provide several replicates
from a single genetic origin, and finally they also minimise
environmental impact by reducing the number of coral colo-
nies collected from the wild. As variability among different
clones of one species can be larger than variability between Fig. 38.15 Plastic basket and mesh (as the ones used in flower shops)
to place the nubbins of the scleractinian corals keeping them in an
species, it is fundamental to work with distinct batches of at upright position and make the transport easy; in the image the basket
least three different genotypes, so that conclusions can be contains Dendrophyllia cornigera nubbins. (Photo: ©A. Veiga)
extrapolated to the species level.
The production of coral nubbins relies on the ability of
corals to propagate asexually through fragmentation the coral to be easily removed and put back in the base. This
(Highsmith 1982). Corals often fragment because of physis particularly useful for experiments that include routine
ical (storms, strong currents) or biological (predators, bio- measurements of respiration and buoyant weight, because
eroders) factors that break off a portion of the colony. these measurements can be affected by the biofilm that may
Coral fragments can also be formed by fission, the conform on the holding bases.
trolled detachment of coral parts as a form of vegetative
reproduction (Lasker 1988). The new fragment is able to
survive and form a new independent colony. Cutting tech- 38.5 Experimentation in Aquaria:
niques or fragmentation follow a similar format. A piece of Increasing the Knowledge
the parent colony is removed using a cutting instrument, on the Physiology and Functioning
and if the cutting is properly removed, it will heal and form of Cold-Water Corals
a new colony similar to the parent colony (Borneman and
Lowrie 2001). This last section of the chapter includes several case studies
Nubbins of scleractinian corals can be prepared by cutting to present the experience of researchers working in the
coral branches of a parent colony with electrician cutters (or Mediterranean region and in the Atlantic with different CWC
bone pliers) previously cleaned in ethanol. Because of their species in aquaria. Using a variety of techniques, different
hard skeletons, coral nubbins can be easily placed in an scientific questions have been addressed, such as how CWCs
upright position, i.e. with coral polyps facing upwards by respond to climate change and other environmental vari-
using a plastic mesh or egg crate (Fig. 38.15). ables, and feeding behaviour and reproduction of
Nubbins of octocorals and black coral can also be pre- CWCs. Each subsection comprises a general description of
pared by cutting fragments with electrician cutters. However, the most common techniques for different types of ecophysi-
because of their fragile, flexible structure, these nubbins ological research on marine invertebrates, application of
require a sturdier base to keep the nubbins upright in aquaria. these techniques to CWCs and a brief description of the main
When preparing nubbins, the outer ramets should be selected findings.
so that there is only one healing point at the base of the nub- Comparative experimental studies of corals require that
bin. Care must be taken to remove the tissue around the axis the environment experienced by each coral fragment is simi-
at the base of the cuttings to avoid it to rot when buried in the lar, except for the studied factor. In the laboratory, for long
epoxy putty. term studies of physiological behaviour, capture rates,
The researchers from the DeepSeaLab in Azores have growth rates or spawning of coral species, it is often neces-
developed specially designed bases composed by an “argo- sary to resemble the environmental conditions experienced
crete” support (composed of cement and aragonite sand) and by the sampled coral as accurately as possible. In addition to
epoxy putty that holds a silicone tube in which the coral supplying a simulated or recirculated flux of water to the cor-
fragment is placed (Fig. 38.16). A small piece of artificial als, temperature controlling this water and ideally the labora-
sponge inside the silicone tube holds the fragment inside the tory, there are several mechanical options available to
tubing without damaging it. This base was designed to allow simulate flow conditions.
Fig. 38.16 (a) Colony of the

gorgonian Dentomuricea aff.
meteor being prepared for
fragmentation; (b) close up of
a nubbin and the bases
described in the text. (Photos:
(a) © A. Godinho, (b) ©
R. Sá da Bandeira)
38.5.1 Measuring Growth and Metabolic CaCO3 g−1 skeleton day−1 or % day−1, the latter method being
Responses of Cold-Water Corals Under suitable for experiments at monthly scales. However, it
Different Environmental Conditions should be taken into account that in case of exponential
growth you cannot use “% day−1” as coral size continuously
Biomineralisation is a major parameter when addressing changes (Leal et al. 2016). One important advantage of TA
effects on the metabolic responses of calcifying species. and BW compared to the use of radioisotopes is that the first
Calcification rate, together with other important physiologi- two are not destructive whereas the latter one is. Estimation
cal descriptors such as respiration, energy acquisition, fecun- of the linear growth extension and sclerochronological tools
dity and gene expression, aim to integrate the organism as a allows a spatial quantification of growth (in mm year−1).
whole in order to characterise the main functions affected Those methods generally require long term experiments
under different environmental conditions. Skeletal growth is owing to low growth rates of CWCs (see for experiments
an energy demanding process, which uses a large proportion with Mediterranean CWCs: Orejas et al. 2011; Naumann
of the energy acquired by corals. The dynamic energy budget et al. 2011, 2013, 2014; Lartaud et al. 2013, 2014; Gori et al.
(DEB) model (Kooijman 1986), is a useful tool to estimate 2014b, 2016), although some species have shown visible
the energy needed for calcification and tissue growth accord- extension after 2 to 3 months in aquaria or in situ (Orejas
ing to the environmental conditions in which the corals live. et al. 2008, 2011; Lartaud et al. 2017a). Finally, quantifica-
Analysis of skeleton pieces also offers the opportunity to tion of the budding rate, which corresponds to the rate of new
investigate growth on a longer temporal scale, as biogenic polyps formed, can be applied as a measure for growth.
carbonates can archive all events that impacted growth dur- These techniques are more relevant for colonial scleractini-
ing the skeleton formation (Schöne 2008; Montagna and ans and octocorals than for solitary CWCs, as for the former
Taviani, this volume). Following this, the use of growth pro- groups the growth is primarily driven by polyp formation
files inferred from sclerochronological analysis can help in a (Lartaud et al. 2017b).
precise dating of growth disturbances after the introduction Recent CWC research conducted in the facilities of the
of new environmental parameters. CSM in Monaco has greatly improved our knowledge on the
For CWCs, several methods are used to measure skeletal ecophysiology of Mediterranean CWC. For example, it was
growth rates in aquaria. These methods differ according to shown that these CWC can tolerate much higher growth tem-
the types of response required (at a global scale or at local peratures than those experienced in situ (12 °C), which sug-
spatial scales on the coral fragments) and the duration of gest that they will be able to cope with summer heat waves
experiments (see chapter by Lartaud et al., this volume). due to global warming (Naumann et al. 2013). Indeed, sev-
Among the main techniques used, the total alkalinity anom- eral species were able to maintain high calcification rates
aly (TA; Chisholm and Gattuso 1991), inclusion of radioiso- when cultured for several weeks at 2 °C–3 °C above their
topes (e.g., 45Ca or 14C; Tambutté et al. 1995; Hennige et al. normal, in situ growth temperatures (Naumann et al. 2014).
2014) and the buoyant weight (BW, Jokiel et al. 1978; Davies Studies have also shown the importance of heterotrophic
1989) provide a quantification of the calcification rate in g feeding in sustaining high calcification rates of the CWC,
Fig. 38.17 Cylindrical
flumes used for feeding
experiments. The motor in the
top of the chambers is
connected to a blade, which
keep the water moving at
constant flow speed. The
speed of the flow can be
switched with the controllers
(white boxes in the right part
of the image). (Photo: ©
C. Orejas)
also suggesting that CWC are more sensitive to starvation Lophelia pertusa from the Mingulay Reef (Scotland, NE
than to temperature increase (Naumann et al. 2011), or the Atlantic) to capture different type of food (copepods, algae,
study conducted with Dendrophyllia cornigera to evaluate particulate organic carbon) at different current speeds. The
the metabolic response of this coral when it relies on dis- chambers consist in 5 L volume cylindrical aquaria equipped
solved organic matter as food source (Gori et al. 2014b). with a paddle which is connected to a motor allowing to
switch to different current speeds (Fig. 38.17); results
revealed a higher feeding rate for this coral species at low
38.5.2 Feeding Experiments with Cold-Water current speeds (2–5 cm s−1) varying the efficiency for the dif-
Corals: Closed and Circulating Flumes ferent food types (for detailed information on the results of
and ‘Mississippi’ Chambers this experiment, please see Orejas et al. 2016.)
For filter feeding sessile organisms with no algal symbionts, 38.5.2.2 Circulation Flumes
movement within the waters surrounding CWCs is essential To the best of our knowledge, the first feeding experiments
for the delivery of food. Flow velocity and reef location performed with Mediterranean CWCs were conducted in the
influence the food that can be delivered to a reef, given the aquaria facilities of the CSM in Monaco in 2008. Four CWC
proximity to a food supply source (such as re-suspended sea- species were used in the experiment: L. pertusa, Madrepora
floor sediments, fresh phytodetritus or a mixed food supply oculata, Desmophyllum dianthus and D. cornigera. Artemia
of phytodetritus and zooplankton). Flow velocity governs the salina nauplii and adults were used as prey items at known
flux and size characteristics of food of different densities or concentrations, revealing different feeding efficiencies for
swimming abilities that can be passively transported to a the four CWC species depending also on the prey size
reef, as well as the ease with which particular coral species (Tsounis et al. 2010). These first experiments were done
can collect this carried food from suspension. Passive filter using small (850 mL volume) closed recirculation flumes
feeders usually show a dome shaped relation between flow (Fig. 38.18) with a constant unidirectional flow (1 cm s−1)
speed and capture rate at a given food concentration (e.g. and they took place simultaneously with the experiments
Hunter 1989; Sebens et al. 1997; Allen 1998; Larsson and carried on with L. pertusa by A.I. Larsson, A. Purser and co-
Jonsson 2006; Wijgerde et al. 2012). With increased flow workers in the Tjärnö Marine Laboratory in Sweden.
speed, the flux of food (food per time unit) delivered to the Purser and co-workers (Purser et al. 2010) considered that
coral increases the feeding efficiency, i.e. the proportion of rather than placing corals in static aquaria or tiny aquaria with
food particles that can be captured and retained decreases at tiny mechanical stirring systems, placing corals in circulating
high flow speeds due to the effect of hydrodynamic forces. flumes could allow a test section (coral mounting area) to be
exposed to unidirectional current at a flow velocity set by the
38.5.2.1 Cylindrical Flumes researcher (Fig. 38.19). Flow was maintained within these
A modified version of the chambers used by Orejas et al. flumes, as already mentioned, by using a rotary paddle, the
(2001, 2003) in Antarctica has been utilised by C. Orejas and speed of which is set manually (Berntsson et al. 2004). Care
co-workers in an experiment to find out the ability of must be taken in the design to ensure that the paddle and drive
Fig. 38.18 Closed
recirculation flume (7 L
volume) used at the CSM to
conduct feeding experiments.
(Photo: © S. Reynaud)
Fig. 38.19 Schematic of a

typical 50 L circulation flume.
This design offers the
possibility for both closed,
recirculation functionality and
operation as a flow-through
system. (Scheme by ©
A. Purser)
shaft are not constructed of materials that can rust due to the speeds, within coral species, among different food items at
salty seawater used in the experimental runs. the same flow speeds, and among different species at the
As shown in Fig. 38.19 these flumes can be used as same flow velocities. Having well defined and documented
closed systems (as it was the case in Tsounis et al. 2010) or flow conditions and food concentrations, is a necessity for
with a continuous flow-through water supply. Commonly, comparison of results obtained by independent studies.
for food uptake studies etc., flumes maintained as flow These flume designs have been useful in demonstrating
through systems may have the flow curtailed for the dura- that different coral species are able to capture food at varying
tion of feeding studies, during which the concentrations of rates under different flow conditions most optimally (Purser
food within the 50 L of water are monitored over a known et al. 2010; Tsounis et al. 2010) and that samples of the same
period of time, so that the capture by the corals within the coral species, collected from locations with considerably dif-
test section can be analysed. Whenever such experiments ferent hydrodynamic and temperature regimes, also collect
are based on monitoring the reduction in suspended food food at differing rates under differing flow conditions. Larger
over time, it is important to also carry out ‘blank’ runs, in flumes such as the 1200 L recirculating flume at Tjärnö
which comparable ‘dead’ coral nubbins are used in the marine station (described in Jonsson and Johansson 1997)
place of live corals, to verify that the corals are indeed can be used to study flow effects on larger pieces of CWCs
responsible for suspended food removal over time, rather or whole coral colonies. This flume has been used to study
than a hydrodynamic trapping factor resulting from the how L. pertusa colonies modify the flow (pattern and veloc-
coral rugosity. Further, it is also important to consider sus- ity) downstream of it, thereby affecting the flux of water and
pended food removed from suspension by corals may not food to neighbouring conspecifics. Further at the CSM, small
actually be consumed by the corals (see Sect. 38.5.3). 7 L volume circulation flumes (Fig. 38.18) have been used in
Following an experimental run, the flow-through system experiments carried out with D. cornigera in order to test
can be restarted. Using a circulation flume ensures the flow how the synergy of different factors (e.g. different tempera-
velocity to be carefully controlled and measured, facilitat- ture and flow speed regimes) influence the capture rate abil-
ing comparison of food uptake rates e.g. among flow ity of this CWC species (Gori et al. 2015).
38.5.2.3 ‘Mississippi’ Chambers the first paddlewheel, mounted in the left-most aquaria in a

Flow conditions surrounding CWCs in the natural situation small plastic mount. With both ends of the paddlewheel con-
may be rather chaotic; both as a consequence of the com- taining magnets, the remaining paddlewheels are attached in
plex relief that may underlie a reef, but also as a result of the a similar fashion via magnetism through the chamber walls.
complex 3D structure that colonial corals may form with This allows the 5 paddles to be rotated in unison, with a fixed
successive generations of growth. The chaotic, turbulent velocity, throughout the 5 chambers making the experimen-
flow can increase feeding rates of corals as the flux and tal unit. Commonly the group have employed 3 × 5 chamber
directions of food delivery are varied, and can also help to Mississippi arrays, to allow 4 × 3 chamber treatments and
minimise deposition of material onto coral structure, as may 1 × 3 control chambers for an experimental run, with the
occur under low flow velocity conditions or under unidirec- various treatments randomised across the 15 chambers. An
tional flow conditions. Turbulent water motion also prevents alternative to using magnets is to use a standard metal bar
the development of surface anoxia on fauna and surfaces, an running through the 5 chambers, with this bar attached
important consideration in long-term or in situ experimental directly to the motor block. With this solution, careful seal-
studies. ing is required to exclude inter-chamber transport of treat-
For in situ benthic experimental work, experimental ments, or the use of a lesser volume of water, i.e. 10 L per
chambers deployable as part of lander systems or operated chamber, to ensure this axle bar remains above the height of
by ROVs, with integrated paddle systems to maintain water the water in each experimental chamber. With this solution
movement were developed by the University of Gothenburg there is a possibility of some bubbles forming during opera-
for general benthic use (Tengberg et al. 2003). These cham- tion, which may have relevance for some treatments or
bers operate by rotating a ‘Mississippi’ type paddlewheel at experimental investigations. A further, more complex design
the top of the chamber by means of a rubber transmission can be made by placing the paddlewheels at 90° to those
belt, which generates a turbulent flow (see Tengberg et al. illustrated in Fig. 38.20. In this case, each paddle is con-
2004). For laboratory work, Jacobs University in Bremen nected by magnets to magnets mounted on a drive chain
modified the design to allow 5 chambers to be run simultane- mounted on the outside of the 5 aquaria. In this case, the
ously with magnetically linked paddlewheels maintaining drive chain turns each exterior magnet ring, which turns the
equal water movement within 5 separated experimental units paddlewheel within each chamber (Larsson et al. 2014).
(Fig. 38.20). Each chamber contains 12 L of seawater, with
either flow-through or static modes possible. Additional
experimental functionality is provided by the attachment of 38.5.3 Carbon and Nitrogen Cycling in Cold-
peristaltic pumps to each chamber, capable of maintaining Water Corals – The Use of Stable
the flow of different additional treatments, such as pollut- Isotope Tracers
ants, food or CO2 enriched waters (Larsson et al. 2013b). The
chambers can also be sealed and used for measurement of The quantification of carbon (C) and nitrogen (N) resource
respiration rates following treatments. A disadvantage of utilisation and subsequent processing by CWCs remains a
using this type of chamber is that the flow conditions and challenging task. Traditional gut content analysis is cumber-
hence the flux of food, sediment etc. are not easily measured some, since scleractinian CWCs are not easy to dissect, and
and defined (will vary with e.g. height of coral, distance from their food resources may consist of small-sized particles, dis-
the corners of the chambers), which makes comparisons of solved organic and even inorganic compounds (Orejas et al.
results among independent studies difficult. 2003; Gori et al. 2014b; Mueller et al. 2014; Middelburg
At the left of Fig. 38.20 the motor block can be seen adja- et al. 2015). In experimental feeding studies, CWCs were
cent to the paddle in the left-most chamber. This motor is offered a range of food types and their ingestion was subse-
connected through the chamber wall by strong magnets to quently measured as the decrease in food concentration or as
the number of food items caught per polyp (Orejas et al.
2003, 2011, 2016; Tsounis et al. 2010; Purser et al. 2010;
Gori et al. 2014b, 2015). Nevertheless, some of the trapped
food may be lost due to sloppy feeding (Moeller 2005; Pitt
et al. 2009) or cannot be assimilated, and thus food uptake
rates may not directly translate to assimilation rates. In addi-
tion, the coral utilises the assimilated food in its total energy
budget (Fig. 38.21), which includes respiration for mainte-
Fig. 38.20 Schematic of an array of replicate 10 L ‘Mississippi’ cham- nance and growth, tissue growth and storage, reproduction
ber aquaria, within which turbulent flow can be maintained whilst pro-
(Davies 1984; Kooijman 1986), calcification (Cohen and
viding a flow-through water supply and timed delivery of experimental
treatments (Scheme by © A. Purser). (For a photograph of a typical Holcomb 2009; McCulloch et al. 2012) and the release of
‘Mississippi’ paddle, see Fig. 38.22) coral mucus as particulate and dissolved organic matter
metabolic activity
13
C/15N – respiration 13
DI C
enriched 13 15
PO C, PO N
resource mucus release 13
DO C
excretion NH4+
15
13
tissue growth 13
C in C in NLFA and PLFA
13 15
& storage coral tissue C/ N in HAA
13
C in NCH
13
reproduction C in reproductive tissue
13
calcification skeletal Ca CO3
Fig. 38.21 Carbon and nitrogen budget of a cold-water coral feeding late organic carbon/nitrogen, NH4+ ammonium, and into coral (repro-
on a 13C/15N enriched resource, from assimilation to utilisation for met- ductive) tissue plus tissue molecules, NLFA neutral lipid-derived fatty
abolic activity, for tissue and skeletal growth and reproductive tissue acids, PLFA phospholipid- derived fatty acid, HAA hydrolysable amino
formation. The resource 13C and 15N can be ‘traced back’ in metabolic acids, NCH neutral carbohydrates, and in skeletal calcium carbonate.
products such as DIC dissolved inorganic carbon, POC/PON particu- (Scheme by © S.R. Maier)
(POM, DOM; Crossland 1987; Wild et al. 2008; Naumann 38.5.3.2 Studies on Food Sources, Selectivity
et al. 2011; Zetsche et al. 2016). The partitioning of the and Carbon Budgets
assimilated C and N amongst these components of the energy SI tracer studies have shed light on CWC physiology in vari-
budget is difficult to determine. ous ways. Mueller et al. (2014) applied SI experiments to test
the ability of L. pertusa to exploit a wide range of 13C- and
38.5.3.1 Stable Isotope Tracer Experiments 15
N-enriched food substrates, including algal-derived amino
to Unravel Organism Physiology acids (DOM), bacteria, phytoplankton and zooplankton. C
Pulse-chase stable isotope (SI) studies are used to quantita- and N of all the tested resources were assimilated into coral
tively follow the uptake and processing of organic and inor- tissue, fatty acids, and amino acids, underlining the opportu-
ganic resources in freshwater and marine organisms nistic feeding strategy of CWCs as a potential adaptation to
(Middelburg 2014) and represent a promising tool to study their variable trophic environment. In addition, de novo syn-
C and N cycling in CWCs. The general principle is quite thesis of individual fatty acids by L. pertusa was apparent
straightforward; an (in)organic C or N resource, with a sub- from the 13C enrichment of individual phospholipid-derived
stantially higher than natural ratio of the heavy isotope (e.g. fatty acids (PLFAs) in the coral, which were absent in the
13
C for carbon and 15N for nitrogen) over the lighter isotope added food sources. This feature may complicate the inter-
(e.g. 12C for carbon and 14N for nitrogen) is offered to the pretation of in situ observations on coral nutrition based on
organism and this ‘heavy isotope’ pulse is used to trace the lipid composition profiles (Mueller et al. 2014).
fate of the resource in the tissue and metabolic products of a van Oevelen et al. (2016) studied selective feeding of L.
consumer (e.g. Middelburg et al. 2000; Moodley et al. pertusa in a cross-labelling approach, providing corals with
2000). 13
C-enriched phytoplankton versus 15N-enriched bacteria and
SI resources can be obtained in various ways: inorganic vice versa; they found no selectivity at low food concentra-
resources (e.g. NaH13CO3, or 15NH4Cl) can be commercially tions and a relative preference of phytoplankton over bacte-
purchased, while organic resources (e.g. phytoplankton or ria at higher food concentration.
bacteria) can be produced by culturing them in a 13C- or 15N-
enriched medium (e.g. Moodley et al. 2000; Mueller et al. 38.5.3.3 Nitrogen Budgets: From Coral
2014). Enriched dissolved organic material (DOM) can be Individuals to the Coral Holobiont
extracted from an enriched algal culture (de Goeij et al. Middelburg et al. (2015) studied the N cycle of the holobiont
2008), while herbivorous zooplankton can be grown by feed- L. pertusa by incubating coral fragments with various inor-
ing them with enriched phytoplankton (Mueller et al. 2014). ganic 15N sources (i.e. ammonium, nitrate and N2).
Surprisingly, the coral holobiont was able to fix N2 gas, (Maier et al. in press.). Studies on OA and temperature rise
which is an energetically costly process, advantageous in could apply the SI tracer methodology to investigate both
periods of N shortage in the deep-sea. Moreover, ammonia changes in carbon budgets of CWCs and reef-associated spe-
was nitrified to nitrate by nitrifying bacteria that are likely cies, and changes in their trophic interactions; assessing the
associated with the coral mucus. The nitrifying community reefs’ recycling capacity and resilience.
used the energy obtained from ammonium oxidation to fix
dissolved inorganic carbon into organic carbon, indicating
chemoautotrophic activity. Also, denitrification activity was 38.5.4 Experimental Research on Cold-Water
observed, which was associated with anaerobic parts of the Coral Reproduction and Larval Rearing
coral gut or with the mucus layer (Middelburg et al. 2015).
At the University of Gothenburg (UGOT) L. pertusa has
38.5.3.4 From the CWC Holobiont to CWC been reared for spawning and larval production since 2011
Reefs: Trophic and Non-trophic (e.g. Larsson et al. 2014), opportunistically starting in
Interactions 2009 when spawning occurred during respiration measure-
Close trophic interactions between reef species, such as ments in a metabolic experiment (Larsson et al. 2013a).
facilitation and recycling of metabolic end products For spawning purposes, the Mississippi chambers devel-
(Fig. 38.21), could represent important reef community oped for previous experiments (see Fig. 38.20, Sect.
adaptations to food or nutrient limitation (Levington 1972; 38.5.2) were modified: individual chambers were made
Richter et al. 2001; de Goeij et al. 2013; Rix et al. 2016). larger to fit the larger coral fragments needed and the back
The application of SI tracers to follow C and N across sev- walls of the chambers were made black so that the whitish
eral trophic levels revealed, amongst others, the assimila- eggs could be more easily detected (Fig. 38.22a). The high
tion of coral-released DOM by sponges, and their turbulence from the Mississippi-type paddles seemed to
subsequent shedding of cellular debris as food source for stimulate spawning behaviour, and kept the corals in gen-
detritivores. This sequence of events has been termed the eral in a good health.
sponge-loop (de Goeij et al. 2013; Rix et al. 2016). Another The parental corals were collected in October–November,
study found that the CWC-reef associated polychaete a couple of months before the estimated local spawning sea-
Eunice norvegica assimilated two to four times more food- son in January–February. The early collection was done to
13
C in the presence of L. pertusa, while corals benefitted allow the corals to acclimatise to the laboratory conditions.
from the polychaete presence by enhanced calcification The collections were carried out with a landing net that was
(Mueller et al. 2013). mounted on an ROV.
38.5.3.5 Outlook 38.5.4.1 Gamete Collection and Fertilisation

SI tracer research on CWCs is in its infancy, but can become In L. pertusa from the NE Atlantic, oogenesis takes a full
an important tool, for example to assess changes in energy year, and somewhat less for spermatogenesis (Brooke and
demand and allocation by CWCs under predicted future ocean Järnegren 2013). Inducing spawning in corals is difficult
scenarios (Cohen and Holcomb 2009). L. pertusa’s allocation (Strathmann 1987), probably since corals do not have ovi-
of food carbon to respiration, mucus production and tissue ducts or sperm-ducts, but see Miller (1996) who induced
growth, including the build-up and depletion of carbon stores, spawning in an antipatharian. Dissecting out polyps to collect
has for instance been addressed in a recent SI tracer study gametes is futile due to discharge of cnidocysts that results in
Fig. 38.22 (a) Small

Lophelia pertusa branches in
‘Mississippi’ chamber with
black wall (b) Larger
branched colony in darkened
‘Mississippi’ chamber.
(Photo: © S. Strömberg)
entanglement and destruction. To induce spawning it would Besides the work conducted with L. pertusa, there are two
probably be necessary to rely on a series of hormones to stim- important papers regarding reproduction and larval ecology
ulate final maturation and tissue breakdown, so the best strat- of Oculina varicosa conducted by Brooke and Young (2003,
egy so far is to allow for spontaneous spawning until complete 2005). Similar data on embryology, larval development,
understanding of the reproductive cycle is achieved. thermal tolerances, and swimming speeds as for L. pertusa is
Lophelia pertusa is a broadcast spawner, and spawning in thus available also for O. varicosa.
laboratory is protracted over 2 months, possibly with one
more intense week during this period. This has yet to be con- 38.5.4.2 Larval Rearing
firmed to also be the case in their natural environment. Larval cultures of L pertusa have been kept in 2–3 L glass
Spawning by males and females were usually synchronised bottles (E-flasks) for maintenance. During the first 3–5 weeks
in chambers where both sexes were combined. Spawning larvae reside in the upper portion of the flasks, swimming
also occurred in chambers where either sex was isolated, underneath the surface, so E-flasks are recommended to be
although, usually never by both sexes the same day in sepa- entirely filled up and kept bottom up to give larvae maximum
rate chamber-sets. If isolated eggs and sperm are needed for volume. If other types of bottles are used, they can be kept
fertilisation experiments, it is recommended that males and horizontal. Regular changes (e.g. weekly) of a fraction (e.g.
females be placed in adjacent chambers that are intercon- 1/3) of the water are sufficient, with occasional larger vol-
nected by a membrane or filter that allows chemical signals umes changed.
to pass between them, but not gametes. It is probably conju- After 10 days, larvae are fully developed planulae and
gated estradiol and testosterone that act as pheromones to good swimmers (see Larsson et al. 2014 and Strömberg
synchronise gamete maturation and spawning (Twan et al. 2016 for further details on development). Feeding should
2006); however, this needs further investigation. start after 20 days—this is when larvae have developed a
Collection of gametes is best done by sucking them up flexible mouth and are ready for foraging. An oral pore is
through 5–7 mm tubing, used as a siphon, into large glass already visible after 2 weeks, but they are not interested in
bowls for fertilisation and embryo development. The bowl food at that point. Larvae seem to be opportunistic feeders
should have a bottom cover of water before transfer. The eggs and prefer a diet similar to adult corals, although, parti-
are approximately 160 μm and barely visible for the naked cles of copepods are preferred over live ones. We have
eye, but they are highly reflective, so with a black background homogenised Calanus sp., centrifuged the homogenate,
and lateral lighting in an otherwise dark room they are easy to and used the fine fraction for feeding. This soup added to
see. Using a sieve to collect the eggs is not possible due to cultures has elicited feeding behaviour, that is, larvae
their delicacy; they simply disintegrate in contact with the swim in a more spiral fashion or stop entirely and move
net, or with surface tension. Eggs and larvae can be handled particles towards the mouth by ciliary movements
with glass pipettes, but water motion should always be kept (Strömberg and Larsson 2017). The carotenoids from the
very slow and gentle. Eggs are initially neutrally buoyant and copepod fragments are also visible through the body wall
spread out in the entire water mass. After fertilisation they of the larvae after feeding, confirming actual intake. Small
become slightly positively buoyant and start to slowly ascend sized microalgae such as Isochrysis sp. and picoplankton
to just below the surface: usually without getting caught in the have also elicited this behaviour, or trailing of mucus
surface tension, unless forced into it by too strong turbulence. strands that food particles adhere to. Larvae have also
Larvae will initially actively swim upwards and gather just been observed to adhere to larger particles of copepods;
below the surface as well (Larsson et al. 2014). either feeding directly off the copepod tissues or from the
If males are less productive and gamete cultures are sperm degrading microfauna or picoplankton associated with the
limited, putting the gamete bowls on a shaking table with tissue.
gentle motion can increase fertilisation success. The friction
of the moving water will increase the water temperature, and 38.5.4.3 Experiments
development rates will therefore increase if embryos are left The experiments that we have undertaken on L. pertusa lar-
on the shaking table as compared with cultures in still water. vae so far have focused on biological and ecological issues.
At UGOT, researchers maintain the cultures, as well as Specifically, we have tried to establish a timeline for devel-
parental corals, at 7–8 °C, since that is the local in situ opment and ontogenic shifts in behaviour during the pelagic
temperatures during the spawning season. They tolerate
phase of larvae to track what is happening from release to
lower temperatures, however, raising the temperatures to settling. This information is crucial to make adequate projec-
10 °C or more usually puts the health of cultures at risk due tions for larval dispersal, as seen in the work of Fox et al.
to increased bacterial growth. The in situ temperature range (2016), where these experimental results were found to
for L. pertusa and other CWCs is 4–12 °C, however, tem- contrast with projections based on assumptions of larvae dis-
peratures above 10 °C have been found to be detrimental in persing as passive particles, with fundamentally different
the long run in aquaria. outcomes as a result.
To elucidate whether larvae reside in the photic zone dur- with filtration units and powerheads to ensure adequate fil-
ing dispersal, we tested if they feed on microalgae, and if they tration and water mixing for each replicate system. L. per-
pass through density layers in the water column (Strömberg tusa fragments were fed a mixture of live Artemia and
and Larsson 2017). The latter may be relevant to the Skagerrak crushed krill (Gamma frozen blister packs) and D. dianthus
area (Northeast Atlantic), where surface waters are affected were fed frozen mysids every 2 days. For more details on
by the Baltic current, and by outflow from the fjords along the the experimental design see Hennige et al. (2015).
coast, which both give a top layer consisting of less saline Considering the current literature available, experimental
water with pronounced haloclines as a result. In most other time scales are very important when assessing whether or not
areas, however, larvae may never encounter lower salinities corals can acclimatise, as short-term experiments may pro-
since offshore oceanic waters usually are not stratified. The duce results (for example a detrimental impact of OA upon
larval behaviour in response to salinity gradients was tested in key processes) that may not appear in longer term studies, as
plexiglas aquaria with a bottom slit, allowing for the slow organisms have undergone alterations in key regulatory pro-
adding of layers of water with different densities. Larvae cesses to acclimatise. This makes it very useful to compare
were then added to the bottom of the aquaria and filmed as both short and long term research, and with regard to L. per-
they swam upwards. These experiments showed that larvae tusa, most significant changes in respiration and calcification
did not react to salinity differences as high as 5 units between occur in the short term (Hennige et al. 2014, 2015), from 24-h
layers, with the top layer salinity as low as 25, instead larvae experiments to 4 weeks. Beyond 4 weeks, decreases in calcifi-
kept swimming upwards until reaching the surface (Strömberg cation and respiration have not been observed in studies to
and Larsson 2017). In addition larvae survived for long even date (see Hennige et al. 2015 and references therein). However,
in a salinity of 25 showing that larvae have a broad salinity even when acclimatisation has been demonstrated, it may
tolerance range. Tests on feeding preferences also show that come at a cost to other processes and may therefore not be
larvae might feed on small size microalgae, although this is sustainable in the long-term. Research in the Edinburgh
not fully verified. In summary, we did not find anything that Changing Oceans facility demonstrated that although growth
excludes the possibility that larvae spend time in the photic rates can continue as normal under low pH conditions over a
zone during dispersal. period of 12 months, skeletal biomineralisation, molecular-
scale bonding and skeletal structure all change. Exposed skel-
eton cannot acclimatise or adapt to future conditions, and its
38.5.5 Experiments with Cold-Water Corals dissolution is a purely biogeochemical process. The dissolu-
under Changing Ocean Conditions tion and weakening of the exposed skeleton observed after
long term OA exposure (Hennige et al. 2015) when combined
The Changing Ocean Group experimental facility in with bio-erosion, may mean that reefs of the future may be
Edinburgh (Fig. 38.10) has been used for two long-term smaller than currently, and consequently unable to support the
projects; (1) impacts of ocean acidification (OA) on L. per- large amounts of biodiversity. The breakdown in the relation-
tusa physiology and biomineralisation (Hennige et al. ship between respiration and calcification in long term experi-
2015), which ran for 1 year, and (2) impacts of OA on D. ments may also indicate that ‘normal’ energetic strategies are
dianthus, firstly for physiological studies (8 months, Gori circumvented in the long-term, possibly due to other processes
et al. 2016) and secondly for biomineralisation research, using energetic reserves (Hennige et al. 2014, 2015).
using pH proxy validation through boron isotopic fraction- Further evidence to support this hypothesis was provided
ation (14 months) (Martin et al. 2016). For these experi- from the study on D. dianthus. Whilst these corals may be
ments, collected corals were fragmented and randomly able to tolerate exposure to acidified seawater, when com-
distributed through all the systems to prevent pseudo-repli- bined with elevated temperature, respiration and calcifica-
cation. For each of the 5 treatments, there were four repli- tion rates decreased. Changes in the ratio of respired oxygen
cate systems, each comprising four 5 L tanks connected to a to excreted nitrogen (O:N) were recorded, indicating that the
60 L sump. Each tank was suitable for holding n = 4 live main sources of energy being metabolised shifted from
coral fragments and a ‘dead’ coral skeleton (80 tanks total). mixed use of protein and carbohydrate / lipid as metabolic
Ambient and elevated CO2 air mixes were bubbled directly substrates under control conditions, to less efficient protein-
into the sump. Experimental conditions for the experiment dominated catabolism under both stressors (Gori et al. 2016).
on L. pertusa replicated ambient and predicted future condi- These results support a growing literature consensus that
tions following IPCC emission scenarios. All replicate CWCs are amongst the most vulnerable of marine ecosys-
systems were housed within a temperature-controlled room tems to global climatic change (Roberts et al. 2016).
at ambient reef temperature, and systems at elevated tem- In the same line as the experiments conducted in
peratures were controlled through Aqua Medic T-computers Edinburgh, J. Movilla and co-workers executed aquaria
and titanium heaters. The bubbled sumps were also equipped experiments in the aquaria facilities at the ICM-CSIC, in
Barcelona in order to assess the response of the skeletal value observed in the sampling area at similar depths and
structure and the tissue composition to OA of four of the used as control conditions, while treatment 2 consisted of a
most widely distributed CWC species in the Mediterranean pH of 7.81 units, simulating the future Mediterranean decline
(L. pertusa, Madrepora oculata, D. cornigera and D. dian- predicted for the year 2100 following an RCP6 scenario
thus; Fig. 38.23). The team developed a system for experi- (IPCC2013, AR5). In this experimental set-up instead to
mental pH manipulation in aquaria that allowed exposing the bubble a CO2 air mixes directly into the sump (Hennige et al.
organisms to different pH conditions, simulating the present 2015), CO2 (99.9% purity) or CO2-free air (using a filter
values and those expected by the year 2100. Movilla and co- filled with soda lime, Sigma Aldrich) were bubbled to either
workers assessed the response of the skeletal structure (cal- increase or reduce pH, respectively. More details in the
cification rate, microstructure, specific microdensity and experimental design and set-up, as well as in the treatments
porosity) and the tissue composition (organic matter amount can be found in Movilla et al. (2014a, b).
and lipids content) in each single species (Movilla et al. For this kind of experiments, it is very important to deter-
2014a, b; Movilla, this volume). mine the in situ values of the carbonate system in the field as
A pH-manipulative experimental system was imple- well as to make a good monitoring of these parameters
mented based on the experimental design described by throughout the experimental phase to check the accuracy of
Reynaud et al. (2003) (Fig. 38.24). The system was installed the treatments. For that purpose, to compare the control
inside a temperature-controlled room to ensure constant val- treatment with the natural range that the organisms experi-
ues during the whole experiment. Seawater was continuously ence in the field, temperature and salinity profiles were
supplied to two 150 L tanks where pH is adjusted to the obtained with a Seabird CTD911 from surface to 400 m
desired experimental values. Treatment 1 consisted of a pH depth, and water samples for pH and total alkalinity (TA)
of 8.10 units (total scale), similar to the current natural pH measurements were taken every 30 m with 24 12-L Niskin
Fig. 38.23 Specimens of

Lophelia pertusa (above left),
Madrepora oculata (above
right), Desmophyllum
dianthus (below left) and
(below right) in the
experimental aquaria. (Photos
from L. pertusa and M.
oculata: © A. Gori; photo
from D. dianthus and D.
cornigera: © E. Obis)
Fig. 38.24 Experimental set-up used to control and modify seawater data logger; (e) solenoid valves; (f) soda lime filter; (g) 50 kg CO2 bot-
pH in each aquarium. (a) and (b) large 150 L tanks for seawater condi- tle; (h) and (i) control and low-pH experimental aquaria, respectively
tioning at pHT 7.81 and 8.10, respectively; (c) glass electrodes for pH (three replicates per treatment); (j) Micro bubble diffusers. (Scheme by
and PT100 probes for temperature measurements; (d) pH controller and © J. Movilla)
bottles mounted in a rosette during a research cruise carried sured at the level of the organism, gene expression profiles
out in the sampling area. revealed considerable changes in response to OA at the cel-
In addition, small volumes of water were taken periodi- lular level. The study showed upregulation of genes involved
cally (once a month during the first 3 months and every sec- in important cellular processes related to calcification and
ond month for the rest of the experiment) to analyse TA by metabolism as a mechanism to counteract the negative effect
potentiometric titration (Pérez and Fraga 1987; Pérez et al. of pH on the coral’s calcification process. This indicates that
2000) and pH using spectrophotometry (Clayton and Byrne CWCs may be able to adjust their physiology in response to
1993), which provides better precision than electrodes. environmental changes as a potential mechanism of acclima-
These values were used to calculate the rest of parameters of tion or adaptation of CWC to OA.
the carbonate system in seawater in both treatments, using Consequently, understanding the molecular mechanisms
the CO2calc software (Robbins et al. 2010). Results of the behind the physiological processes involved in a coral’s
experiments have been already published and can be found response to elevated pCO2 is critical to assess the ability of
in Movilla et al. (2014a, b) and Movilla (this volume). CWCs to acclimate or adapt to future OA conditions.
38.5.5.1 Gene Expression Studies with Cold-

Water Corals in a Changing Ocean 38.5.6 Measuring Effects of Drilling and Oil
While the above mentioned studies have mostly focused on Spills in Cold-Water Corals
studying the effects of OA at organism-level (e.g. growth,
calcification, metabolism), only Carreiro-Silva et al. (2014) Cold-water corals are often found in association with hydro-
have looked at the impact of OA at the molecular level of carbon drilling areas. Offshore drilling activities discharge
gene expression. For zooxanthellate corals, molecular tech- large amounts of waste materials into the water column that
niques looking at gene expression have produced useful cause increased sedimentation around oil and gas installa-
insights into understanding the physiological pathways tions. The discharged drill cutting material is made up of the
involved in the response of corals to OA, by targeting genes rock cuttings generated during drilling and attached added
involved in the cellular stress response, biomineralisation, drilling fluids (Holdway 2002). For CWC reef fauna, there is
and energy metabolism (e.g., Kaniewska et al. 2012; Moya great concern is over the potential for drill-cuttings to cause
et al. 2012; Vidal-Dupiol et al. 2013). Indeed, the studies of smothering (Roberts et al. 2006), and coral mortality has
Carreiro-Silva et al. (2014) on the impact of OA on D. dian- been observed in the immediate vicinity of drilling discharge
thus have shown that although elevated pCO2 did not cause points (Gass and Roberts 2006). Another evident risk is oil
significant changes in calcification or respiration rates mea- spills, which, unlike drill cutting discharges, are accidental.
Following the 2010 Deepwater Horizon disaster in the Gulf that will end up on vertically and horizontally oriented parts
of Mexico, where an amount of oil equal to approximately of the coral will depend on the coral morphology, the weight
4.4 million barrels of oil was released (Camilli et al. 2010), and stickiness of the sediment particles, and the water veloc-
several oil-impacted coral communities were studied in situ ity with more sediment particles settling from above at lower
(White et al. 2012; Fisher et al. 2014). Except for the crude flow velocities. Exposure to suspended sediment particles
oil, coral communities were also exposed to a chemical dis- for a period of time requires appropriate equipment. Brooke
persant added into the wellhead in order to mitigate the con- et al. (2009) exposed L. pertusa fragments to suspended sed-
sequences of the oil spill (DeLeo et al. 2016). iments in closed recirculating systems for 2 weeks. Slurry of
There are two main ways of exposing corals to sediments, sediment was introduced at the start of the experiment and
either by letting the sediment settle onto coral surfaces in the water with suspended sediment was pumped from the
water with low or no movement (e.g. Larsson and Purser conical bottom of the experimental aquarium to the top
2011; Allers et al. 2013) or by (periodically or continuously) ensuring water circulation and that sediment particles were
exposing the corals to suspended sediment particles in mov- kept in suspension. Both Brooke et al. (2009) and Larsson
ing water (e.g. Brooke et al. 2009; Larsson et al. 2013b). In et al. (2013b) regularly monitored the sediment concentra-
the first case with settled sediments, only ordinary aquaria or tion in the experimental aquaria. In Larsson et al. (2013b), L.
jars are needed for exposure. Since the surface area of the pertusa was exposed to natural benthic sediments and drill
aquarium floor is known, a slurry of sediment can be added cuttings continuously during a period of 3 months
for targeted exposure of sediment mass per unit area. If a cer- (Fig. 38.25). The corals were kept in constant flow through
tain burial depth is aimed for, pre-tests of resulting sediment of water in “Mississippi” chamber aquaria (Fig. 38.20) and
depth on the aquarium floor from known sediment loads may sediments were added to the aquaria by the use of peristaltic
be necessary. Flow through of water is turned on after the pumps from stock solutions with specific concentrations.
sediment has settled. Such aquaria experiments have shown Sediment particles in the stock solution were kept in suspen-
that L. pertusa actively removes both natural sediment parti- sion by circulation pumps. Constant sediment exposure in
cles and drill cuttings through ciliary movements on the ten- the aquaria was reached by balancing the flow through rate
tacles (Zetsche et al. 2016) and through mucous shedding on of water with the delivery rate of sediment stock solution.
tissue covered parts of the skeleton (Allers et al. 2013; Zetsche The internal circulation of water in the aquaria was governed
et al. 2016). Repeated exposure does not affect the cleaning by the paddlewheels (Fig. 38.20). By maintaining sufficient
efficiency but sediment can accumulate on tissue-free (bare) flow through of water and sediment, the settlement of parti-
skeleton and after repeated exposure cause smothering of cles onto corals and other structure in the aquaria was com-
adjacent tissue and polyps (Larsson and Purser 2011). paratively very small and the particle concentration could be
When corals are exposed to suspended sediment particles kept constant. Results showed that sediment accumulates
in moving water, the degree of exposure is depending on the also onto vertically oriented surfaces of coral fragments,
sediment flux, i.e. on the concentration of sediment particles starting at tissue-free parts, which may result in smothering
times the flow velocity. For the same sediment concentration, of polyps. Skeletal growth can correspondingly be slightly
the exposure in the flow direction is hence twice as high adversely affected after months of exposure (Larsson et al.
when the flow velocity is doubled. The amount of sediment 2013b).
Fig. 38.25 Experimental
set-up for long-term exposure
of Lophelia pertusa to
suspended benthic sediments
and drill cuttings. Experiment
performed at the University of
Gothenburg marine station at
Tjärnö, Sweden. (Photo: ©
A. I. Larsson)
38.5.7 The Fragile Chemical Equilibrium

in Cold-Water Corals Maintenance:
An Example from the Levantine
Mediterranean Sea
This section reports a few notes and comments on how an

almost catastrophic and irreversible loss of tissue of
Dendrophyllia ramea colonies kept at the Ocean Aquarium
in Cyprus was prevented. The coral colonies were collected
off Cyprus at around 150 m depth in a soft bottom habitat.
This is the first time that D. ramea has been recorded in the
Mediterranean Sea at such a remarkable depth and in a sedi-
mentary environment (Orejas et al. 2017).
The aquarium hosting the coral colonies had one ton of
seawater with a “sump filtration system”. This particular set-
up allows for efficient filtration of the aquarium water in a
way that the chemical and biological parameters are precisely
and fully controlled. Technicians in charge of the coral exhi-
bition performed daily routine checks, such as chemical water
analysis and temperature control, to ensure the right aquarium
conditions for the corals. Feeding was performed with a
syringe, separately to each colony, to minimise food waste
and to increase the feeding efficiency of the polyps. Despite
the efforts of technicians, 4 months after the corals were on
display, an outbreak of filamentous algae was noticed, which
infested the whole aquarium within a matter of days. Later
on, technicians also observed a sudden and significant regres-
sion of live tissue and polyp size and the expansion of fila-
mentous algae on the bare skeleton (Fig. 38.26a, b). An
experienced aquarist revealed that the infestation and tissue
loss was the result of a sequence of events that occurred due
to poor water quality, incorrect lighting (that favors algae pro-
liferation) and insufficient nutrition. The corals were exposed
to increased levels of phosphates, and insufficient nutrition,
which may have affected growth and calcification. The con-
tracted polyps suggested a weakening of the polyps.
Concurrently, increased levels of nutrients (phosphate and
nitrate) and excessive illumination exposure of the aquarium
promoted the growth of filamentous algae. With the corals Fig. 38.26 The evolution of the Dendrophyllia ramea colonies in the
weakened and the filamentous algae proliferating in the public aquarium of Protaras after an infection event. a) healthy D.
aquarium, it was a matter of time for the filamentous algae to ramea colonies when first transferred in the aquarium facility (June
2015), b) colonies already highly infected by the filamentous alga inva-
aggressively colonise the coral skeleton and lead to notice- sion, c) Cerithium spp. gastropods were introduced in the aquaria to
able coral tissue loss. Once corals reached this health status, graze the algae, d) polyps of D. ramea covering again the coral skele-
it was almost irreversible and the death of the coral colonies ton. (Photos: © V. Andreou)
was apparently imminent. Technicians, always in close col-
laboration with the specialist, attempted to limit the infesta- Hence, it was decided to place the corals in a quarantine
tion using simple, non-invasive techniques. By increasing the tank while the main exhibition tank was disinfected using
frequency of water changes, water quality was rapidly chemical agents (Fig. 38.26c) to remove the filamentous
increased with minimal impact on the corals. Although the algae that were still present. This procedure was followed
outbreak was prevented from further infestation, filamentous as most of the chemical agents that could be used to elimi-
algae were still present in the aquarium exhibition and the nate filamentous algae are harmful to most invertebrates
health state of the corals did not change. Improved water and corals in particular. After completion of the disinfec-
quality on its own proved to be a weak treatment and time was tion procedure, corals were transferred back to the main
running out as more coral tissue was lost during this process. exhibition aquarium. Since many variables may have
played a role in the development of the filamentous algae, fish compounds was positive and immediate: they were
changes in the aquarium set-up were also performed in ready to capture the mysids that were given individually
order to avoid similar incidents in the future. The original to each individual polyp with a syringe.
lighting system was replaced with one of a specific wave After the successful treatment following the steps men-
length that limits photosynthesis, in order to inhibit fila- tioned before (regulation of nutrient concentration in the
mentous algae growth. Additionally, two “wave maker” water, lighting, cleaning by the gastropods and a better diet
pumps that simulate alternate underwater currents were more in agreement with the nature of the Dendrophyllidae
installed in the aquarium and the previous UV filtration species), a significant improvement in the coral colonies was
system was replaced with a larger unit that can circulate observed. The size of the polyps increased and there was a
water at a higher rate. These were precautionary measures progressive increase or recovery of lost tissue. At the moment
to further enhance coral health. of writing this there is an incipient polyp budding within a
Despite the efforts of the technicians and the successful few areas of healthy tissue.
removal from the aquarium system of the filamentous algae Aside from the aspects presented in this chapter regard-
and cyanobacteria, at this stage the infestation on the coral ing the importance of research in aquaria to shed light in
skeleton persisted and so was the tissue loss. Once the water the biology, ecology and physiology of CWCs, we would
quality was optimal and monitored regularly, the persistence like to stress out the paramount role that exhibitions in
of filamentous algae on the coral skeletons can be attributed public aquaria also have to disseminate the existence and
to surrounding lighting. Despite the fact that the lighting unit importance of these habitats and communities, and to
of the aquarium hosting the corals was replaced, lighting of transmit this message to the society. The dissemination of
the adjacent aquariums and the maintenance area behind the research is still an unfinished business for many scientist,
aquarium might have provided sufficient lighting for the sus- particularly for the CWC research (see Rossi and Orejas,
tenance of the filamentous algae. this volume). Aquaria exhibitions play a fundamental role
Not being able to treat coral skeleton in the same way on this and numerous scientific institutes and public
as the aquarium (the disinfection procedure is deleterious aquaria around the world are starting to contribute to this
to living organisms), it was necessary to identify the algae by planning “open door” days as well as allocating spe-
and bacteria (cyanobacteria) that were progressively cific areas dedicated to deep-sea fauna.
expanding on coral skeletons. Once identified, a signifi-
cant number of Cerithium spp. gastropods were intro- Acknowledgements We acknowledge the following projects for their
duced into the tank with the corals. These benthic species, support to these studies: FP6 HERMES (EC contract no.
GOCE-CT-2005-511234), FP7 HERMIONE (Grant agreement No.
which were collected from the rocky shoreline in the 226354), CoCoNet (Contract no.287844) programmes, as well as
vicinities of the aquarium, have a specialised diet consist- ASSEMBLE TA project (grant agreement no. 227799), Statoil funded
ing of different unicellular algae, particularly diatoms, as CORAMM project, EVER-EST Horizon 2020 project (contract no.
well as biofilm forming cyanobacteria. A few days after 674907), DG Environment programme IDEM (grant agreement No
11.0661 /2017/750680/SUB/EN V.C2), Chaire ‘Extreme environment,
the introduction of Cerithium in the tank, the basal sec- biodiversity and global change’ (Foundation TOTAL and UPMC),
tions and branches of the corals exhibited areas free of CoralChange project (contract no. 231109) and the Flag Project Ritmare
algae, corresponding to the areas where the gastropods Ricerca Italiana per il Mare. Further projects are CYCLAMEN funded
had gathered and grazed-clean the skeleton without affect- by the TOTAL foundation (BIO_2014_091_Juin_CS-8), the European
Project LIFE Indemares ‘Inventario y designación de la red natura 2000
ing the remaining live tissue (Fig. 38.26). en áreas marinas del estado español’ (LIFE07/NAT/ E/000732), the
Because of the significant volume loss experienced by Spanish Project DEEP CORAL (CTM2005-07756-C02-02/MAR) and
the polyps while they were retracted due to the algal infes- the Acciones Complementarias (CTM2005-24174-E, CTM2006-
tation, it was attempted to promote recovery by optimis- 27063- E/MAR, CTM2007-28758-E/MAR). These works has also
received funding from the European Union’s Horizon 2020 research
ing the coral diet. Different feeding types were tested, as and innovation programme under grant agreements No 678760
well as an increase in the percentage of mysids (small size (ATLAS) and No. 689518 (MERCES). This output reflects only the
crustacean) and copepods in the diet. Both groups are author’s view and the European Union cannot be held responsible for
common prey for Dendrophyllidae corals. This alternative any use that may be made of the information contained therein. The
funds provided by the Fundação para a Ciência e a Tecnologia (FCT,
diet substituted the regular one based on soft tissue with- Portugal) through the strategic project (FCT/UID/MAR/04292/2013)
out exoskeletons from other decapods and bivalve mol- granted to MARE are also acknowledged. This is ISMAR-Bologna sci-
luscs. In order to stimulate polyps’ capture reaction, fluids entific contribution n. 1940. We are very grateful to Dr. Ronald Osinga
and micronised tissue of fresh fish with high fatty acids and Dr. Simonepietro Canese who thoughtfully and enthusiastically
reviewed this chapter providing such insightful suggestions that would
were added to the water in the tank before the actual feed- have been rightfull to make co-authors of the chapter.
ing with the alternative diet. The polyps’ reaction to the
Some European Research Institutes and Public Aquaria References

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Drop Chapter
Approaching Cold-Water Corals 39
to the Society: Novel Ways to Transfer
Knowledge
Sergio Rossi and Covadonga Orejas
Abstract was a vast underwater desert. CWC ecosystems have been

Outreach is fundamental to disseminate scientific knowl- one of the most neglected ecosystems on earth, being its
edge and approach the general public. The cold-water functioning and role unknown for decades. For most people,
coral ecosystems are not an exception. During the last the biodiversity, complexity, biomass and the life explosion
15 years many efforts have been made to make more in the surroundings of these live three dimensional structures
familiar these complex ecosystems to the society. was unexpected; although CWC are possibly one of the more
Technology (which allow the possibility to reach deepest widespread ecosystems of the world, comparable in distribu-
locations) but also the engagement of scientists made this tion and biomass to shallow coral reefs (Roberts et al. 2006).
approach possible. In this short contribution we highlight Only in the last three decades the scientific research field on
several ways to promote the knowledge and the sensitisa- CWC started to be relevant. The attention paid to these com-
tion on these fragile deep water ecosystems, showing pre- munities was associated from the beginning to the fact these
vious experiences and discussing some ways to effectively fragile ecosystems are being deeply transformed by humans
transfer the information needed to protect and manage and these changes are taking place faster than the proper
these fragile ecosystems. identification and mapping of these ecosystems (Hinz 2017).
Indeed, the animal forests living on the deep (formed by
Keywords scleractinians, gorgonians, sponges, bryozoans, etc.), are
Scientific knowledge · Dissemination · Cold-water corals being damaged and sometimes completely devastated at a
· Mediterranean · Outreach · General public · Ocean rhythm that we, scientist, cannot overtake with our surveys
literacy and studies (Koslow et al. 2001; Rossi 2013). The direct and
powerful actions of scientific outreach opened a window to
the society, allowing a better interpretation of the role and
functioning of CWC, offering in an easy way basic informa-
The Discovery of Cold-Water Corals tion, fundamental for undertake a sustainable management
to the Society and conservation for the present and for the future.
Until the middle of last century almost no one (but see the
old work by Pontoppidan 1755) was talking about cold-water ome Examples on Cold-Water Coral
S
corals (CWC), and indeed the general image of the deep-sea Scientific Outreach
S. Rossi (*) During the last decade, the number of outreach outputs on
DiSTeBA, University of Salento, Lecce, Italy CWC has grown exponentially (Fig. 39.1). Different research
Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma groups made a huge effort to make available visual and “easy
de Barcelona, Cerdanyola del Vallés, Spain to manage” information for the general public. In Alaska,
e-mail: [email protected] Canada and the West Coast of the United States for example,
C. Orejas pioneering institutions made an important attempt to wide-
Instituto Español de Oceanografía (IEO), Centro Oceanográfico de spread images and information through different actions. In
Baleares, Palma de Mallorca, Spain

https://doi.org/10.1007/978-3-319-91608-8_39
474 S. Rossi and C. Orejas
Fig. 39.1 Different
dissemination materials of the
Cold-water coral (CWC)
ecosystems. (a) brochure
published by OCEANA to
disseminate the need of
protection for the
Mediterranean CWCs,
(credits: © OCEANA) (b) the
web page www.lophelia.org,
which aim to disseminate
scientific knowledge, news
and provide education
material about CWCs (credits:
© lophelia.org), (c) cover of
the publication “Cold-water
corals- Out of sight not longer
out of mind” (UNEP), this
was one of the first
publications to disseminate
the basic knowledge on the
CWC communities, (credits:
© UNEP) (d) Model of a
scientific submarine
constructed by the scientist
from the ICM-CSIC (Credits:
© Project “El Mar a Fondo”,
www.elmarafondo.com)
Alaska, the MESA program promoted by the NOAA (e.g. mate change, together with the possible expansion of oil
https://www.afsc.noaa.gov/ABL/MESA/mesa_me_cor.php) exploitation in these areas, are problems which have been
made visible their results about the impacts on CWCs in this quickly disseminated thanks to such blogs, which have been
area, and in Canada also the government made a direct effort essential to contribute to the sensitisation of local and non-
to make more visual the existence and the threats to CWC local people toward the conservation of these deep commu-
(e.g. http://science.gc.ca/eic/site/063.nsf/eng/h_EE39B64D. nities, which became very urgent. A clear example is the
html). The Monterrey Bay Aquarium was one of the first Arctic Sea Ice Forum (https://forum.arctic-sea-ice.net/)
institutions to make an exhibition of sessile and mobile spe- where posts of different specialist and non-specialists show
cies of the Monterrey submarine canyon, adapting aquaria to different views in different formats about the rapid changes
the deep-sea species (Sims 1998), being actually very suc- in the Arctic areas. A similar strategy (blogs and outreach
cessful (Sims pers. comm.). The positive response of the papers) was also recently used for the dissemination of the
public encourages other aquaria in Europe to follow the same Mediterranean CWC in the INDEMARES Life + project
example (Laterveer et al. 2008). (http://icmdivulga.icm.csic.es/) and the CYCLAMEN proj-
In some cases, dynamic internet blogs in which people ect (http://cyclamen.cyi.ac.cy/), explaining the threats and
could directly ask basic questions about the deep-sea com- the recent discover of some of these CWC communities (see
munities were also very successful. For example, the rapid Gori et al., this volume; Orejas et al., this volume) as well as
changes that polar areas experience as a consequence of cli- their relevance to the general public. Also within
39 Approaching Cold-Water Corals to the Society: Novel Ways to Transfer Knowledge 475
INDEMARES it is worthy to mention the very nice (and artistic way as a new manner to transfer knowledge (Fig. 39.2,
very successful) initiative promoting the vision (with a real https://medwavesblog.wordpress.com/wow/).
size model) of a scientific submarine. In this project, people Non Governmental Organisations (NGOs) like
could get inside this submersible and visualise underwater Greenpeace, OCEANA or the World Wildlife Found
videos recorded on CWC communities from the (WWF) are very active disseminating the scientific knowl-
Mediterranean (Fig. 39.1d). edge on CWC communities. They made an excellent work
The effort made by scientists has been the key to make showing the impacts of the trawlers in these seafloor com-
visible the problems and the conservation initiatives to main- munities, giving the chance to the people to see what we
tain the CWC ecosystems. Former European projects as cannot (and sometimes we do not want…) see. These
ACES, HERMES, HERMIONE or CORALFISH, among actions carried out by NGO’s which implies the display of
others, were fundamental to increase the knowledge on these fantastic videos and photos showing the beauty of the cor-
ecosystems and in some cases also for the declaration of pro- als which act as architects of these deep-sea communities
tected areas beyond the coastal zones. These “pioneer” ini- are very effective tools to make people aware on the exis-
tiatives working in deep-sea areas, were an important basis tence of these communities and to sensitise for their protec-
for current European projects such as, for instance, ATLAS tion. Further quite a lot of the dissemination activities to
and SPONGES. The European large projects are deeply present the CWCs to the society are a join action between
committed contributing to enlarge the number of mapped scientist and NGOs, as it can be seen in pioneer documents
areas in the deep-sea as well as providing the know-how on as the “Cold-water coral reef. Out of sight – no longer out
different aspects of the biology and ecology of these fragile of mind” (Fig. 39.1), which was a collaborative work
ecosystems. All these efforts have been translated in updated between a large group of scientists, governmental agencies
and fully informative web-pages in which scientific informa- and NGOs (Freiwald et al. 2004).
tion, but also outreach and new ideas are presented including Contributing to increase the relevance and impact of the
a high visual and aesthetic component (e.g. www.lophelia. outreach actions is an important task which is being taken
org/, Fig. 39.1b). In the United States, there are also many seriously by many CWC researchers as well as by govern-
and very good examples of outreach programs. For instance mental organisations and NGOs. We present here two cases
the NOAA used also a good informative vector (reports but which exemplify different way to act and present to the gen-
also easy to visualise web pages) that helped the general eral public some of the threats that put the CWC ecosystems
public to understand not only the CWC of US waters but also in risk. The first case we present here deal with the effects of
the functioning and potential/current threats derived from bottom trawling in these communities, and the second one
different anthropogenic impacts (Lumsden et al. 2007). For with the effects of oil exploitation in the oceans.
instance the inputs of NOAA scientists in the web pages (e.g. Deep-sea fisheries industry has grown almost exponen-
http://ocean.si.edu/ocean-news/deep-sea-corals-noaa-educa- tially during the last two decades (FAO 2016), especially in
tion-plans-activities) are a valuable information source for the bottom trawling sector. Sound scientific background
conservation organisations as well as for other research insti- produced by different universities and research institutes as
tutes (https://blog.marine-conservation.org/2017/05/the- well as surveys and explorations conducted by NGOs have
hunt-for-a-super-coral-can-cold-water-corals-adapt-to- been playing over the years an equally fundamental role
ocean-acidification.html). presenting the CWC and its paramount role as ecosystem
YouTube has become one of the probably most powerful engineers to the society. These actions have highly influ-
tools to reach the general public, and especially to target enced governments and institutions of a high political level,
young people. The implementation of videos including very as it is the case of the EU parliamentary which undertook
short (2–4 min) stories contribute to “put in the map” the actions towards trawling ban at the beginning of this decade.
presence, biodiversity and fragility of these systems. Indeed after a long debate, the EU supported the banning of
Frequently scientists are reluctant in using “funny” and bottom trawling beyond 800 meters depth in most of the EU
visual tools to show their findings, since they are concerned waters (MEPs ban deep-sea fishing below 800 meters in the
that these activities might trivialise the scientific results. North-East Atlantic, December 2016). This achievement has
However, this step has become essential to reach many peo- been the result of a long process which started in 2005 and
ple who are interested in to learn but are used to obtain infor- reaches the first agreements in 2011 for depths below 1000
mation through “fast channels”. Further the use of other meters; however this is still the allowed limit for bottom
ways to transmit knowledge, as art, is a powerful tool which trawling in Mediterranean waters, which means that many
works not at the level of “facts” but at the “emotional” level. species are still under threat as confirmed in the recent pub-
Humans are sensible to beauty and the use of other channels lication by the IUCN presenting the current status of the
needs to be further explored. A recent dissemination project Mediterranean anthozoans (Otero et al. 2017; see also Otero
called Ways of the Waves (WoW) explores the visual and and Marin, this volume). Especially the bamboo coral
Fig. 39.2 Outreach-artistic
project to disseminate
scientific knowledge gain
during the scientific cruise
MEDWAVES, conducted in
frame of the European project
ATLAS. Images (a–c)
correspond to fotograms from
different video clips which
can be visualised under
https://medwavesblog.
wordpress.com/wow/, (d)
correspond to a series
photograms from one of the
video clips which represent in
an artistic and poetic way the
relation between the water
masses from the
Mediterranean and the
Atlantic. (Credits: Images by
© Martha Zein and © José
Luis Matoso)
Isidella elongata has been categorises as “critically endan- which endanger these communities and the need of mitiga-
gered” (www.iucnredlist.org/initiatives/mediterranean), the tion actions (Figs. 39.3 and 39.4).
species has also been recently included in the Annex II of Exploration of the deep-sea floor to extract oil and min-
Barcelona Convention. The depth limit for bottom trawling erals is a potential threat for CWC (Clarke et al. 2010)
has been changed and moved to shallower waters over the which is currently taking place in many locations, included
years. In these negotiations, there has been a clear influence the Mediterranean, and it would not stop during the next
of the sound scientific evidence of mismanagement in deep years (Murton 2013; see also Otero and Marin, this vol-
areas, as well as by the dissemination made by several ume). Dissemination of the consequences of oil spills in the
NGOs on the consequences of this mismanagement of the ocean has been a fundamental tool to show to the public the
deep-sea ecosystems (Aguilar et al. 2017). The ban of bot- consequences of accidents as the one originated by the
tom trawling at certain depths and in certain areas is an “Deep Sea Horizon oil spill” in the Gulf of Mexico (GoM).
excellent example of how the synergy of different actions Beside the tragic human casualties, a strong negative impact
from different groups and at different levels contribute to of this oil spill on the coast and the deep-sea communities
make people aware about the importance of an ecosystem as was documented (Prouty et al. 2016). The already available
the one dominated by CWCs, making evident the threats information on the CWC communities of the GoM thanks to
Fig. 39.3 Different ways to

disseminate the effects of
bottom trawling in the
seafloor. (a, b) campaign by
“Bloom association” to
promote the ban of bottom
trawling (credits: © Bloom);
(c, d) images from the
Mediterranean Sea where the
effects of bottom trawling in
the bamboo coral Isidella
elongata populations can be
observed, white arrows show
in image “c” colonies
dislodged from the substrate
and image “d” the path of a
trawl mark an a single I.
elongata which survive
(credits: © OCEANA); (e)
poster published by FAO to
help fishermen and scientist to
recognise the most frequent
CWC species from the
Mediterranean. The poster is
freely available by FAO
webpage (credits: © FAO)
previous published investigations (e.g. Brooke and Some Thoughts About Scientific Outreach
Schroeder 2007; Cordes et al. 2008; Brooke and Ross 2013)
and the currently available technology to revisit the deep The lack of awareness by the general public on the deep-sea
benthic ecosystems of the GoM, allowed to obtain precise ecosystems in general and CWC ecosystems in particular is
information of the catastrophic scenario and obtain visual due to the remoteness of these ecosystems which have been
documentation of it which was obviously the best “weapon” elusive to most people, more than any other ecosystems of
to engage stakeholders, government and society to under- our planet. It cannot be forgotten that the technology needed
take immediate research activities and mitigation actions. to get access to these deep-sea areas is expensive and acces-
The already existent background information on these CWC sible just for a small groups of researchers and some NGOs,
ecosystems was essential to obtain the quick response from making difficult to have a “feeling”, for these areas as a citi-
the society and the sensitisation of the people of the area zen. Nevertheless, these aspects cannot be the only reason
(see for example www.lophelia.org/latest/338-dwh, and for being not well informed...a common problem is also the
http://response.restoration.noaa.gov/about/media/bottom- lack of interest from many people and the failure from the
gulf-mexico-corals-and-diversity-suffered-after-deepwater- scientist to transfer in a proper way the knowledge.
horizon-oil-spill.html).
Fig. 39.4 Two different

campaigns to disseminate the
effects on the ecosystems of
the exploitation of the
deep-sea species. (Credits: ©
OCEANA)
This lack of interest is frequent regarding many scientific people who are the “future society” and will need to cope
fields. It is not easy to find the “magic formula” to do good with the world we are leaving them...they will need to cope
and high quality dissemination, creative and precise at the with the threats to the CWC communities and they will have
same time, but nowadays is evident, as demonstrate by the to develop the proper tools to solve it...all impossible without
two specific cases we presented before, that public awareness proper information; (2) those who “pay the taxes”...hence...
is essential. A deep knowledge of the current status of the every citizen which at the end rely on sound scientific infor-
CWC communities as well as the problems and threats they mation which will help to build their own opinion in front of
are experienced today is necessary to develop outreach strate- the importance of these communities, their sustainable man-
gies that can reach stakeholders and policy makers, but also agement and the associated threats and conservation prob-
the citizens. Everyone should be targeted when planning out- lems, and (3) the policy makers which also need the scientific
reach actions and we can identify three specific groups which information but in an highly and feasible applied way which
required different efforts, focus, and ways to envisage out- can help them to put “numbers” and “facts” to the issues, as
reach from our side, as scientists: (1) children and young these are the tools they can use to define management and
protection strategies. There are many actions on CWC out- address the current problems that threat the planet (Dayton
reach targeting the first two groups: one of the pioneer and and Sala 2001). The new generations of scientists frequently
very visual, intuitive and high quality webpage for CWC dis- focus in a very specific research question or topic, which
semination: www.lophelia.org/fun-stuff, or www.earthrang- make sometimes difficult to understand the “big” question
ers.com/wildwire/bbtw_updates/why-you-should-protect- behind their small spot of study. We talk about recovery and
cold-water-coral/). These kinds of initiatives are increasing at stability of habitats, but do we really know when they are
different regional levels, from the local ones to country and stable, when and how they can recover? (Bianchi et al. 2017).
also European level (Helvarg 2006). Regarding dissemination We need to be prepared to try to ask the right questions,
activities addressing policymakers, the approach need to be which come from a deep and unhurried observation of eco-
necessarily different. The idea behind considering that the systems and nature. We need to transmit to the new genera-
only possible economic and social model is continuous tions this approach. Undoubtedly, the exploration of the deep
human growth population and expansion is based on a very ocean in general and the CWC in particular will be a vast
“western byassed conception” of our environment (Jacques field to find inspiration.
et al. 2008). At the end of the day, nothing has unlimited grow
(maybe with the exception of corals?), economist will have Acknowledgements We are grateful to OCEANA, Bloom association,
much more to say about that, than we, simple biologists. Our Prof. Murray Roberts (www.lophelia.org) and the project “El Mar a
Fondo” (Fundació La Caixa) for the images we use to illustrate this
perception is that the current model is destined to fail (Rossi chapter. Thanks also to two the reviewers Claudia Pichler and Rana Abu
2019). Taking the CWC as an example, and especially in such Alhaija for her constructive and useful comments. This work has been
a restricted environment as it is the Mediterranean, a system partially supported by the ATLAS project. This project has received
where exploitation of the oceans (e.g. high fishing effort, bot- funding from the European Union’s Horizon 2020 research and innova-
tion programme under grant agreement No 678760 (ATLAS). This out-
tom contact fishing gears, mining and drilling) and direct put reflects only the author’s view and the European Union cannot be
indirect anthropogenic effects (e.g. presence of microplastics held responsible for any use that may be made of the information con-
everywhere, global change including ocean acidification) tained therein. This work is contributing to the ICTA “Unit of
does not have a proper management, it has no chances to sur- Excellence” (MinECo, MDM2015-0552). This drop chapter is dedi-
cated to the memory of Félix Descalzo.
vive. Consequently, it is urgent to change our mind, and con-
tribute to change the mind of the society as CWC ecosystems
are especially complex, diverse and fragile.
Scientists have to undertake actions at local and country References
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Part III
Future
Perspectives of Biophysical Modelling
with Implications on Biological 40
Connectivity of Mediterranean
Cold-Water Corals
Matthew W. Johnston and Ann I. Larsson
Abstract global modeling examples will be given for species that

Biological connectivity of marine organisms that repro- reproduce in a similar fashion. It is hoped that these
duce via planktonic larvae, such as cold-water corals, is examples can provide insight into the future usage of bio-
regulated by the reproductive and life history traits of the physical modeling to study Mediterranean cold-water
organism and by physical characteristics of the marine corals as their characteristics and the physical influences
environment into which offspring are released. that shape their population connectivity are better
Connectivity across vast seascapes enables the persis- understood.
tence of metapopulations over ecological and evolution-
ary timescales and is important when planning the Keywords
conservation and management of vulnerable species Biophysical models · Connectivity · Population connec-
impacted by overfishing, habitat destruction, or invasive tivity · Source-sink dynamics · Modeling · Larval
species. To study marine connectivity of these organisms, dispersal · CWCs · Life history traits
researchers typically measure genetic population struc-
ture or use computer modeling, the latter often using bio-
physical models which integrate both the physical
processes of the ocean and the biological traits of the 40.1 Introduction
study species. Herein, a broad overview of biophysical
modeling topics will be presented including source-sink The life cycle of many marine benthic organisms includes a
dynamics and model parameterisation, paradigms, uses, pelagic larval stage that in part enables their connectivity
and examples. Unfortunately, there is limited availability among populations. Connectivity across vast seascapes
of basic life history data on Mediterranean cold-water enables the persistence of metapopulations over ecological
corals, which are required to implement such models. and evolutionary timescales (e.g. Gaines et al. 2007) and
Known biological traits that are important for dispersal knowledge of the biological and hydrodynamic factors that
and connectivity are therefore here summarised for cold- determine connectivity are fundamental when planning the
water corals found in the Mediterranean and elsewhere. conservation and management of vulnerable species
The traits are discussed in context of dispersal potential impacted by overfishing, habitat destruction, or invasive spe-
and their potential use as parameters in biophysical mod- cies (Treml et al. 2012; Andrello et al. 2013; Johnston and
eling studies of dispersal. Very few such studies of cold- Purkis 2015). For populations in the deep-sea, knowledge of
water corals have to date been performed and none of these factors is especially important. Methods used for some
them in the Mediterranean, therefore as a complement shallow water species, e.g. marking and recapture of larvae,
are not possible to use in the deep-sea and sampling of mate-
M. W. Johnston (*) rial for e.g. genetic structuring is logistically difficult and
Halmos College of Natural Sciences and Oceanography, very expensive. In the case of cold-water corals (CWCs),
Guy Harvey Research Institute, Nova Southeastern University, understanding connectivity may be particularly important to,
Dania Beach, FL, USA for example, predict the potential for recovery of reefs fol-
lowing mechanical destruction by deep-water dredging from
A. I. Larsson fishers and to establish marine protected area (MPAs)
Department of Marine Sciences, Tjärnö Marine Laboratory,
University of Gothenburg, Strömstad, Sweden networks. Although there is a great demand for biophysical

https://doi.org/10.1007/978-3-319-91608-8_40
484 M. W. Johnston and A. I. Larsson
model studies of CWC connectivity, only a few recent stud- between 350–600 m (Taviani et al. 2011). These corals are
ies have been performed (Cardona et al. 2016; Fox et al. sessile as adults and the to-date studied species propagate
2016; Ross et al. 2017). This can largely be explained by lack via current-diffused sexually produced larvae (Waller and
of biological data for deep-sea organisms that can inform the Tyler 2005; Larsson et al. 2014; Feehan 2016; Martinez-
dispersal models (Davies and Guinotte 2011; Hilario et al. Quintana et al. 2015). Unfortunately, there is limited infor-
2015). mation on the reproductive behaviors, larval traits, and
There are numerous biological factors controlling popula- general life histories of CWCs in the Mediterranean, there-
tion connectivity of benthic marine species such as CWCs fore the known biological traits that are important for dis-
including the pelagic larval duration of the offspring (hereaf- persal and connectivity of CWCs found in the Mediterranean
ter PLD – the period of time a larva remains in the water are here summarised and complemented with information
column from spawn until recruitment), reproductive strategy, on CWCs found elsewhere on the globe. Data of this kind
larval buoyancy and motility behavior, and life-stage mortal- are needed to adequately parameterise biophysical models
ity (Cowen et al. 2006; Treml et al. 2012, 2015; Boavida that can be used to study connectivity of CWCs. Very few
et al., this volume; Reynaud and Ferrier-Pagès, this volume). such studies have been performed to date and none of them
Physical environmental conditions, such as the speed and in the Mediterranean.
direction of water flow, salinity, and water temperature, are To recognise the usefulness of biophysical modeling as it
also important drivers of connectivity and enable the persis- pertains to the understanding of connectivity of CWCs, it is
tence of metapopulations over time (Guizien et al. 2012; first necessary to gain an understanding of (1) the aim of
Treml et al. 2012; Johnston and Purkis 2015; Fox et al. biophysical models themselves, (2) population ‘sources’ and
2016). Methods used to study connectivity in the marine ‘sinks’, and (3) the drivers behind biological connectivity.
environment include larval marking and recapture (Jones Given the paucity of studies specific to CWCs, referenced
et al. 2005), otolith microchemistry (Swearer et al. 2003), here are interwoven global examples of biophysical models
genetics (Hedgecock et al. 2007; Boavida et al., this volume used to study other marine organisms. These examples can
and references therein), and biophysical modeling (Verdier- illustrate the importance of biophysical models in under-
Bonnet et al. 1997; Cowen et al. 2000; Guizien et al. 2006; standing marine connectivity and the implications of various
Kool et al. 2010; Johnston and Purkis 2015; Fox et al. 2016), biotic and physical processes on model results. They also
which is the focus of this chapter. Each of these methods has demonstrate how the models may be useful to study CWCs
predictive strengths and weaknesses and when considering in the Mediterranean as more becomes known about these
CWCs, only genetic data and biophysical modeling are plau- inhabitants of the deep.
sible methods to use. In particular, genomics are often relied
upon by biologists as a method of studying marine organism
connectivity and provide an overarching understanding of 40.1.1 The Aim of Biophysical Models
how populations are connected over evolutionary timescales
(Hellberg et al. 2002; Palumbi 2003; Boavida et al., this vol- The deep CWC ecosystem and their population complexity
ume). For e.g. colony-forming CWCs where individuals can necessitate an understanding of both the biological and phys-
be very long-lived, the connectivity patterns found may how- ical realms in order to emulate their marine seascape niche
ever be purely historical (further elaborated under Sect. and their dispersed populations. Individually, biological and
40.1.1 below). Biophysical dispersal models have the advan- physical models aim to reproduce natural conditions and to
tage of using present known distributions of organisms and provide insight into the function of natural systems through
contemporary oceanographic conditions to predict connec- synthetic simulation. In a strictly physical model that may
tivity, given present habitat layout or changes in habitat examine CWC connectivity for example, information about
structure in the future. Biophysical modeling of an organism water flow and source location would be incorporated but the
over multiple generations can also be useful to elucidate larvae would be treated as passively-diffused particles, while
decadal connectivity patterns of populations and infer bio- biological influences, such as planulae movement, would be
logical and genetic connectivity. Results from generational discounted or not considered (e.g. Siegel et al. 2003; Rossi
models can be contrasted with genetic population connectiv- et al. 2014). Subsequently, the data produced by such a
ity studies (Liggins et al. 2013); however, models over mul- model would be limited and not fully descriptive of the true
tiple cohorts are generally uncommon as optimising model state of nature, given that larval movement (i.e. directional
parameters is highly complex and only a few solutions have behavior, especially vertical migration) may influence con-
been proposed (Guizien and Bramanti 2014; Hernandez nectivity (Paris et al. 2007). Biological connectivity models
et al. 2014). in contrast largely ignore the physics of water motion and
The focus of this book is Mediterranean CWCs, which instead focus solely on the biological drivers of connectivity
are deep-water cnidarians that live mostly at aphotic depths such as reproductive traits, suitable habitat congruity, and
40 Biophysical Modelling and Connectivity of Mediterranean Cold-Water Corals 485
various life-stage mortalities (e.g. Thorrold et al. 2002). test the model by varying the biological and physical param-
Neither method is complete. eter values to test model assumptions. Section 40.3 discusses
Moreover, many biologists measure connectivity derived the various implementations of marine biophysical models,
solely from DNA studies. Genetic connectivity studies but first a dialog on population sources and sinks and bio-
though do not reveal the intricate mechanics of dispersal and logical and physical drivers of biological connectivity pro-
instead evaluate the status of a population over various time vided next is prudent to establish context.
scales, depending on the genetic markers used (Cowen and
Sponaugle 2009). In the context of many marine populations
(including CWCs) that may be under duress from multiple 40.1.2 Population Sources and Sinks
immediate stressors such as disease, environmental damage,
or invasive species (Galil, this volume), understanding con- A population source, when considering the biological con-
nectivity over decadal or sub-decadal timescales is impor- nectivity of benthic marine organisms such as CWCs, is a
tant. Since populations of many CWC species expand population of organisms in a location that produces propa-
through colonial growth and asexual reproduction through gules (i.e. spores, eggs, coral planulae, etc.) that are subse-
fragmentation, genets (genetic individuals) can be very long- quently dispersed via water flow to other locations. These
lived, i.e. thousands of years (Dahl et al. 2012). By occupy- propagules from a source population may be carried either
ing space, these individuals limit new recruitment, resulting short or long distances on ocean currents or be retained near
in gene flow blockage (Padrón and Guizien 2016). As such, the natal organism, resulting in relatively open or closed
it is difficult to discern between contemporary and historical populations (Cowen et al. 2000). In corals, traits such as
genetic connectivity, although present technical develop- brooding and crawling planulae (e.g. the cold-water octo-
ment will improve this possibility (Boavida et al., this vol- corallian Drifa glomerata, Sun et al. 2010a) will promote
ume). Understandably, for long lived species like CWCs, retention and aid in local population self-recruitment whereas
genetic connectivity estimates could mirror historical pat- traits such as broadcast spawning, vertical migration of lar-
terns with extinct stepping-stone populations that previously vae, and a long PLD (e.g. the cold-water scleractinian
connected geographically distant populations, and to e.g. Lophelia pertusa, Strömberg and Larsson 2017) will increase
establish MPA networks based only on such connectivity dispersal distance by taking advantage of water flow gradi-
estimates could be disastrous. The aim of biophysical mod- ents (Paris et al. 2013). Effects of reproductive strategy and
els in the context of CWCs would be therefore to integrate larval traits on dispersal will be further discussed in Sect.
biological and physical methods, given that both are likely 40.2.1 below.
equitable drivers of connectivity, to deliver a more realistic A population sink is a location that receives propagules
representation of the functionality of CWCs in the short- and from a nearby or distant source population. Once arriving at
long-term perspective. Ideally, these seascape genetic studies a sink location either via passive or active transport, propa-
could then incorporate biophysical modeling to provide a gules of sessile organisms that recruit to the benthos usually
more holistic picture of connectivity of CWCs (Liggins et al. remain there throughout their lifetime. It is important to
2013; Buonomo et al. 2017). understand that source and sink locations may be the same
Advances in computational power now allow researchers (i.e. self-recruitment), a location may be solely a source or a
to approach the subject matter of marine population connec- sink, or a location may function as both a source for one
tivity using computing power to run complex particle track- location and a sink for another. For example, a CWC inhabit-
ing algorithms – something not possible just a few decades ing a deep-water escarpment off of Cyprus may retain 100%
ago. Indeed, with decent simplification of intricate mechan- of its larvae through nearshore eddies, may export all propa-
ics, it is possible to run complex models on a modest laptop gules offshore and solely rely on distant coral colonies to
computer. However, complexity also increases uncertainty in recruit to the ledge, or there may be a gradient of bi-
interpreting the results and introduces potential error. Given directional exchange between two locations.
this, modern biophysical models are prone to model assump-
tions and so most models integrate a limited number of phys-
ical and biological components that are deemed the most 40.2 D
rivers of Marine Biological
critical from each discipline in an attempt to simulate a natu- Connectivity
ral system (Hernandez et al. 2014). Attempting to account
for all variables is unreasonable and can introduce bias to the To understand biophysical models, it is imperative also to
synthetic model system by including components that may discuss the biological and physical drivers of marine bio-
not be biologically or physically relevant (Warren and Seifert logical connectivity and especially those which researchers
2011). To mitigate such errors, an important component to use to parameterise biophysical models. Marine benthic
any study implementing a biophysical model is to sensitivity- organisms such as CWCs exhibit a significant range of
fecundities, reproduction modes, propagule behaviors, mor- The fecundity of a few CWC species that appear in the
talities and lifespans that help enable the persistence of pop- Mediterranean have been investigated. Populations of
ulations over generations. These life history traits compose Desmophyllum dianthus in Chilean Patagonian fjords show
one primary driver of biological connectivity in ocean sys- high fecundity compared to other deep-sea scleractinians,
tems. A primary driver of connectivity is also the physical with an average number of eggs per polyp ranging from 2500
environment itself, such as ocean water flow, temperatures, to 170,000 among fjords (Feehan 2016). In northeast Atlantic
salinity, bathymetric composition, and water depth. While populations, Waller and Tyler (2005) measured the fecundity
the physical and biological components are an intricately in Lophelia pertusa as 3300 oozytes per cm2 skeletal area
woven tapestry and their individual influences cannot which was an order of magnitude higher than 256 oocytes
always be easily extracted, they will be treated separately per cm2 in Madrepora oculata. Preferably, the fecundity
here to aid in explanation and interpretation. Additionally, should be investigated in several different geographical areas
the traits and conditions below are not an exhaustive list; since optimal environmental conditions may differ between
they were selected based on those parameters that are pre- CWC-species and fecundity will vary accordingly.
dominately used in biophysical modeling at the time of this
writing. 40.2.1.2 Mode of Reproduction and Time
of Spawning
Corals have two sexual reproductive modes which largely
40.2.1 Biological Traits determine their dispersal potential. Scleractinian reef-
forming CWCs studied to date, i.e. Oculina varicosa,
40.2.1.1 Fecundity and Maturity Solenosmilia variabilis, Goniocorella dumosa,
Organisms that produce large quantities of larvae may show Enallopsammia rostrata, L. pertusa, M. oculata, and D.
greater biological connectivity between source and sink dianthus, are broadcast spawners (Brooke and Young 2003;
locations than those organisms which produce fewer off- Burgess and Babcock 2005; Waller and Tyler 2005; Larsson
spring or breed only sporadically. This is because, on the bal- et al. 2014; Pires et al. 2014; Feehan 2016) – i.e. eggs and
ance of probabilities, a greater number of offspring that are sperm are released into the water column where fertilisation
produced increases the chances of successful recruitment, and embryo development take place. Most solitary CWC
assuming equal predatory pressures on planktonic larvae of scleractinians (Waller 2005; Waller and Tyler 2011; Mercier
all species. Still, there exists a vast knowledge gap about lar- et al. 2011; Waller and Feehan 2013) and perhaps a majority
val predation and how this may affect model uncertainty. of cold-water octocorals including all deep-sea sea pens
Note also that metapopulation growth and persistence (Rice et al. 1992; Tyler et al. 1995; Eckelbarger et al. 1998;
increase with reproductive output, though dispersal distance Orejas et al. 2002, 2007; Pires et al. 2009, Mercier and
may not (Treml et al. 2015). Concordantly, organisms that Hamel 2011, Beazley and Kenchington 2012; Baillon et al.
mature at an earlier age also may contribute offspring to the 2014; Feehan and Waller 2015; Rossina et al. 2017) are also
larval pool sooner and perhaps greater quantities over their broadcast spawners. In contrast, for brooding species, fertili-
lifespan than those that mature later (Johnston and Purkis sation of eggs occurs either in or on the surface of maternal
2016). Similar to increased fecundity, early maturity may colonies and larvae are mature before released. Among stud-
enhance biological connectivity between regions for species ied CWCs, hydrocorals (Brooke and Stone 2007), some soli-
exhibiting this trait, at least in the short term. It must be bore tary scleractinians (Waller et al. 2008) and some octocorals
in mind, however, that some late-maturing species produce (Cordes et al. 2001; Orejas et al. 2007; Sun et al. 2009,
copious amount of eggs after sexual maturity and are long- 2010a, b; Mercier and Hamel 2011; Grinyó 2016) are brood-
lived, perhaps offsetting the disadvantage of late maturity ers. The larvae of broadcast spawning corals generally have
when contrasted with quick-maturing species (Johnston and greater potential to disperse widely outside their natal reef
Bernard 2017). whereas brooding corals release mature larvae directly that
The age of maturity is to our knowledge not estimated for are ready to settle within much shorter periods (Harrison and
any true CWCs but there are some indications that polyps Wallace 1990; Underwood et al. 2009). Although “mode of
need to reach a certain size before becoming reproductive reproduction” cannot be fed directly into a biophysical dis-
(e.g. Feehan 2016) and that larger colonies have more fertile persal model, it is a proxy for the length of the larval pre-
polyps (Sun et al. 2010b). However for deep-water alcyona- competency period – i.e. the minimum period of time that
cean octocorals of the genus Drifa, Sun et al. (2010a) report larvae disperse in the water column before settlement. For
that colonies only a few centimeters in size are fertile. The brooded larvae, this period is very short, from a few hours to
youngest fertile colonies of the Mediterranean octocoral a few days in tropical species (Harii et al. 2002 and refer-
Corallium rubrum sampled at 40 m depth by Torrents et al. ences therein). Generally, brooders also exhibit shorter
(2005) were 7–10 years old. median PLDs (Underwood et al. 2009). The effect on disper-
sal of larval pre-competency period and PLD is further periods than those of their broadcast spawning relatives and
discussed below. Only recently, the reproduction mode of shorter pre-competency periods are coupled to shorter
two deep living Mediterranean gorgonian octocorals has median PLDs (Underwood et al. 2009). Some brooded lar-
been investigated. Both Paramuricea macrospina (Grinyó vae are however also capable of settling after many weeks
2016) and Eunicella cavolini collected at 70–100 m depth (reviewed by Harrison and Wallace 1990), so the maximum
are internal brooders. The previously investigated gorgoni- PLD can still be quite long enabling occasional long distance
ans C. rubrum and the facultative zooxanthellae Eunicella dispersal in brooding coral species (Underwood et al. 2007,
singularis which have both shallow and deep populations are 2009).
also internal brooders (Gori et al. 2012; Martinez-Quintana There are very few studies of CWC larval biology.
et al. 2015). Planulae of two brooding NW Atlantic octocorals of the
Knowledge about the time of spawning is also crucial to genus Drifa settle from 1 day up to 3 months after release in
model coral larvae dispersal since the circulation of water temperatures of −0.5 to 8.5 °C (Sun et al. 2010a). Brooke
masses within a sea basin differs with seasons (e.g. Hayes and Young (2003) studied larval development of the
et al., this volume). For seasonally reproducing CWCs, broadcast-spawning facultative zooxanthellate coral O. var-
spawning is speculated to be coupled to seasonal fluctuations icosa that forms extensive reef systems along the edge of the
in quality and quantity of food (Burgess and Babcock 2005; Florida shelf at 70–100 m depth. Larvae in this study were
Waller and Tyler 2005; Sun et al. 2010a, b; Mercier et al. reared at 25 °C and a ciliated planula formed 9 h after fertili-
2011; Brooke and Järnegren 2013). Lophelia pertusa repro- sation. The larvae initially swam upwards but started to
duces annually, with differences in timing depending on show benthic-probing or creeping behavior after 1–2 weeks
geographical location. Spawning occurs in Jan-March in the signaling maturity to settle, and settling was observed after
NE Atlantic (Waller and Tyler 2005; Brooke and Järnegren 3–4 weeks. Larval development was comparatively much
2013; Larsson et al. 2014), in Sept-Nov in the south-eastern slower in L. pertusa from the northeast Atlantic with a fully
US and Gulf of Mexico (Brooke et al. 2007; Brooke and developed swimming planulae formed 9 days after spawn-
Järnegren 2013), and in May–July in Campos Basin off ing (Larsson et al. 2014). Larvae were reared at in situ tem-
Brazil (Pires et al. 2014). Reproduction of D. dianthus has peratures of 8 °C and a recent study show that when the
only been studied in Chilean fjords but also shows strong rearing temperature is increased to 11–12 °C, the develop-
seasonality with gametes likely spawned in August – i.e. at ment rate approximately doubles (Strömberg and Larsson
the end of the austral winter (Feehan 2016). Contrasting to L. 2017). The difference is likely caused by an upturn in meta-
pertusa and D. dianthus, M. oculata produces multiple bolic rate with temperature, and highlights caution when
cohorts annually (Waller and Tyler 2005; Pires et al. 2014). inserting available data of pre-competency periods and PLD
Although these three species are common in the into biophysical dispersal models. Lophelia pertusa is a cos-
Mediterranean, reproduction in these corals is not yet studied mopolitan species found at various depths and at both low
here. The deep living Mediterranean gorgonians E. cavolini and high latitudes and consequently its embryos and larvae
and P. macrospina (Grinyó 2016) reproduce annually and may encounter a large range of temperatures. This species
earliest in July and August respectively. typically thrives at 4–12 °C (Rogers 1999), but appears in
water masses of ca. 13 °C in the Mediterranean (Taviani
40.2.1.3 Precompetency-Period and Pelagic et al. 2017). Since larvae also exhibit ontogenetic vertical
Larval Duration (PLD) migration and possibly migrate into surface waters
The larval precompetency-period determines the minimum (Strömberg and Larsson 2017), the temperature span
amount of time that embryos and larvae, after being released, encountered may be even larger. In conclusion, it is impor-
spend in the water column before maturing to settle. The tant to consider the ambient temperatures at various reef
precompetency-period is hence equal to the minimum sites and the effect it may have on larval development rate
pelagic larval duration (PLD) period for coral planulae. and larval duration.
Considering the chances of larvae settling locally – i.e. in the The precompetency period of L. pertusa planulae reared
vicinity of the natal reef – the pre-competency period is more at 7–8 °C is at least 3 weeks as indicated by the observation
instrumental than the maximum length of the PLD. A short of cnidocyst discharge starting 20 days after spawning, and
pre-competency period will increase the proportion of larvae the use of these for temporary attachment to the substrate
recruiting locally (e.g. Harrison and Wallace 1990; (Strömberg 2016). Earliest notation of bottom probing
Underwood et al. 2009; Treml et al. 2015). The dispersal behavior is also at 3 weeks of age (Larsson et al. 2014) but
potential outside the natal area increase with PLD and for the majority of larvae start showing this behavior at
both median and maximum dispersal distance, PLD is most 4–5 weeks or later (Larsson et al. 2014; Strömberg and
important (Treml et al. 2015). As discussed above, planulae Larsson 2017). No settling of L. pertusa planulae is yet
of brooding corals generally have shorter pre-competency observed but larvae can survive for a full year in laboratory
cultures indicating a possibly very long PLD in this species rate biophysical modelling of larval dispersal. Several studies
(Strömberg and Larsson 2017). have found major effects of vertical migration on both dis-
Larval ecology of deep water corals in the Mediterranean persal distance and connectivity (e.g. Fiksen et al. 2007;
is poorly investigated but Martinez-Quintana et al. (2015) Paris et al. 2007; Corell et al. 2012; Moksnes et al. 2014; Fox
studied planulae from shallow populations (25–30 m) of the et al. 2016), and for deep-sea organisms the effect of being
brooding octocoral C. rubrum. This coral has been found to transported in the surface layer compared to deeper layers
800 m depth in the Mediterranean (Freiwald et al. 2009). can be dramatic (Young et al. 2012; Fox et al. 2016). The
Larvae maintained at 19–21 °C had a maximum PLD of most direct and accurate way of finding out where in the
42 days (Martinez-Quintana et al. 2015). Since larvae also water column larvae reside is to collect larvae in the field at
were active swimmers with a clear upward swimming behav- different depths as done by Arellano et al. (2014) for deep-
ior, the authors conclude that the dispersal potential in open sea molluscs. While this is possible, it involves extensive
waters should be high. This hypothesis is contradicted by sampling efforts in expensive field surveys, during the period
molecular studies of shallow populations showing significant when larvae are in the plankton. Unlike mollusc larvae that
gene flow only on very limited spatial scales (Costantini wear a shell, deep-sea coral planulae are soft-bodied and
et al. 2007; Ledoux et al. 2010). This pattern may however be prone to disintegrate when filtered out from the seawater. It
explained by that C. rubrum is a heavily harvested species would therefore demand genetic screening of species-
fragmenting the metapopulation (e.g. Tsounis et al. 2013). specific DNA sequences to verify presence, a scientific
methodology still in its infancy. Amplification and charac-
40.2.1.4 Embryo and Larval Behavior terisation of genomic DNA from tissue of L. pertusa planu-
In addition to pre-competency period and PLD, the realised lae has previously been successfully performed (Larsson
dispersal distance can be significantly influenced by embryo et al. 2014) indicating such sampling could be feasible.
and larval behavior. Traits such as embryo and larval buoy- As an alternative, the probable in situ depth distribution
ancy, larval type (crawling or swimming) and swimming during different larval phases can be deduced from larval
behavior will decide where in the water column larvae are behavior in laboratory experiments – i.e. the tendency of
transported during their different life phases. Some brooding positive or negative buoyancy, active vertical swimming and
corals release non-swimming planulae (crawlers) that onset of bottom probing behaviour. Using data and observa-
depending on the ambient current strength may be trans- tions from Larsson et al. (2014), Ross et al. (2017) made a
ported a very short distance before they settle from the water “vertical migration profile” for L. pertusa planulae, which
column and become demersal. Such an example is the deep- they used as input to model the dispersal among a network of
sea alcyonacean octocoral Drifa glomerata (Sun et al. MPAs in NE Atlantic. Larsson et al. (2014) observed that L.
2010a). With crawling larvae, recruitment is often restricted pertusa larvae accumulate in the upper part of aquaria until
to within a few hundred meters from the parental colonies 3–5 weeks old and Strömberg and Larsson (2017) (see also
(e.g. Harii and Kayenne 2003). For broadcast spawning cor- Orejas et al., Chap. 38, this volume) further showed that
als, embryo density dictates if they are positively or nega- 4–5 weeks old planulae that were introduced at the bottom of
tively buoyant, which for CWCs can be extra critical since aquaria consistently reacted by swimming upwards until
the development to swimming larvae can take several days reaching the surface. The larvae also passed salinity gradi-
(Larsson et al. 2014). Brooke and Young (2003), noted that ents with a maximum tested difference of 5 with no hesita-
eggs of O. varicosa are negatively buoyant. In contrast, eggs tion (Strömberg and Larsson 2017). Larvae were further
of L. pertusa appear to be neutrally buoyant, and embryos observed to feed and survived for months also at salinities
from one-day old, positively buoyant (Larsson et al. 2014). typical for surface waters above coastal populations in the
In addition, L. pertusa embryos start developing cilia Skagerrak (25). This indicates that the larvae may spend a
three days after fertilisation and are slowly ascending swim- period of their pelagic phase in the photic zone, being trans-
ming blastulae after five days. After an inactive phase when ported in the relatively faster surface currents, before
gastrulation occurs, larvae are competent swimmers at the descending to settle. Ontogenetic shift in vertical positioning
age of 7–9 days (Larsson et al. 2014). was also observed by Brooke and Young (2003) in O. vari-
Although most marine larvae are weak swimmers, many cosa. When planulae became ciliated they swam to the sur-
of them are able to regulate their vertical position in the face of the water where they resided for about a day before
water column, which may change over time (ontogenetic turning to swimming actively throughout the water column
shifts) or with diel or tidal cycles. Other determinants of ver- during 1–2 weeks. The above findings suggest that CWCs
tical position are larval buoyancy and vertical water flow. may take advantage of surface currents for dispersal (similar
Since both the current direction and velocity normally differ to many marine benthic organisms) and therefore is an inte-
with depth (Sponaugle et al. 2002), knowledge of the posi- gral behavioural component that should be included when
tion of larvae in the water column is crucial for more accu- using a biophysical model to examine CWC connectivity.
40.2.1.5 Mortality genetic differentiation among the regions provided that lar-
Natural life stage mortality is likely the second most influen- vae are primarily dispersed by currents at the depth where
tial to PLD in the context of maintaining biological connec- they are spawned. This hypothesis was corroborated in a
tivity of benthic marine species between regions in later study by Miller and Gunasekera (2017) where popula-
biophysical models (Johnston and Purkis 2016). Marine tions of D. dianthus were clearly genetically structured by
organisms are arguably most vulnerable to predation (i.e. the depth rather than by geographical location. These results
‘wall of mouths’ theory – Hamner et al. 1988), disease, and suggest planulae of D. dianthus may not migrate vertically as
simply death in the larval stages of their life – perhaps planulae of L. pertusa do (Strömberg and Larsson 2017) but
reflected by the large number of offspring that most small there are no larval observations available for D. dianthus.
marine fauna produce. Even a small percentage reduction in Similar to Miller et al. (2010), Becheler et al. (2017)
mortality during the egg or larval phases can produce a much found contrasting patterns of connectivity between the CWC
more robust next generation cohort (Johnston and Purkis species L. pertusa and M. oculata. These two reef-building
2016). This is because reduced larval mortality allows a species often occur together in the northeast Atlantic and
greater number of individuals to have the opportunity to suc- were here studied in continental slope canyons of the Bay of
cessfully colonise, likely increasing biological connectivity Biscay. Genetic structuring was detected among the five can-
between regions. We suggest that decreased larval mortality yons spanning a distance of ~500 km for populations of M.
is perhaps a partial explanation for the success of non-native oculata whereas L. pertusa was panmictic on this scale.
species, whereas larvae ‘released’ from predation in their Because the coral species co-occur in all the canyons studied
introduced range allows a large percentage of spawned lar- by Becheler et al. (2017) hence sharing the hydrodynamic
vae to reach adulthood. Natural mortality (i.e. not including environment, and sampling of corals has been conducted in a
fishing pressure) generally peaks during recruitment and is similar way, it is likely that one or several of the biological
commonly at its lowest point after full maturity (Ware 1975). parameters important for dispersal of larvae differ between
Unfortunately, empirical measures of larval mortality these species. Since both species are broadcast spawners,
under natural conditions for most marine organisms includ- other traits must underlie the difference. There is a large dif-
ing CWCs are scarce despite its high importance for disper- ference in fecundity between these species with L. pertusa
sal outcomes (Treml et al. 2015). Mortality rates of larvae having more than 10 times higher fecundity than M. oculata
under laboratory conditions will not reflect mortality rates in in studied northeast Atlantic populations (Waller and Tyler
the field where e.g. predation is an important controlling fac- 2005). Given the genetic structuration of M. oculata occur-
tor. On the other hand, many bacteria and parasites flourish ring at a smaller scale than in L. pertusa populations, we may
in closed laboratory cultures, artificially shortening the life hypothesise that planulae of M. oculata (which are not yet
span (Strömberg and Larsson 2017). In laboratory cultures, studied) have a shorter pre-competency period, and/or a
these authors noted a 60% survival rate of developed L. per- shorter pelagic larval duration period (PLD). But other
tusa planulae during a 3-month period, though it is unknown explanations could be a different vertical migration pattern
how representative this is of mortality in the wild. (if any) or the time of spawning (Treml et al. 2015) due to
e.g. differences in hydrodynamical conditions among sea-
40.2.1.6 Reproductive and Larval Traits, sons, since L. pertusa reproduces seasonally whereas M.
and Implications for CWC Connectivity oculata produces two cohorts annually in northeast Atlantic
The importance of differences in reproductive and larval waters (Waller and Tyler 2005). Hopefully the larval biology
traits is highlighted by genetic estimates of connectivity of many more deep-sea coral species can be studied in the
among deep-sea coral populations, which have shown future to help explain such differences in connectivity pat-
species-specific variation. Miller et al. (2010) assessed con- terns among CWCs and that can be integrated into future
nectivity among nine deep-sea coral species populations on biophysical modeling efforts.
seamounts and slopes in the Australian and New Zealand
region spanning thousands of kilometers. They found con-
flicting estimates of connectivity with evidence of genetic 40.2.2 Physical Ocean Conditions
subdivision among regions for three of the species whereas
levels of genetic variation were low for the remaining spe- The physical environment into which the offspring are
cies. The authors hypothesise that differences in larval biol- released is equally as important as species traits in driving
ogy of which virtually nothing is known for the studied population connectivity. Following is an audit of environ-
species may explain the observed differences in connectivity mental ocean conditions that influence biological connectiv-
patterns. For the estimated low connectivity in D. dianthus, ity and that are commonly used to parameterise biophysical
Miller et al. (2010) also suggest that differences in sampling models. We also direct the reader to chapters Hayes et al.,
depth of this coral may have contributed to the observed this volume and Chimienti et al., this volume, which contain
a comprehensive review of biogeography of CWCs and rents (West coast of Italy, the Northern Current along France
physical ocean conditions in the Mediterranean that are and Spain) dominate the circulation pattern.
important drivers of CWC populations. As it pertains to general trends that would be seen in a
biophysical modeling study of CWCs, typical intermediate
40.2.2.1 Ocean Currents water circulation in the Mediterranean suggests that connec-
The predominant physical driver of biological connectivity tivity should increase from east to west across the basin for
for benthic organisms that reproduce via pelagic marine lar- CWCs with neutrally or negatively buoyant larvae. However,
vae is water flow (Treml et al. 2008; Cowen and Sponaugle surface water flow, where larvae of the CWC L. pertusa may
2009). In some regions such as the western Atlantic and Gulf be contained, does not necessarily reflect deep flow, particu-
of Mexico, dispersal is heavily influenced by very swift and larity in the western Mediterranean where biophysical mod-
persistent surface currents such as the Loop Current and Gulf els have suggested an eastward flow of buoyant larvae
Stream. Many marine larvae including some CWCs (e.g. L. (Johnston and Purkis 2015).
pertusa – see Sect. 40.2.1) vertically migrate, or are buoyant Notably, and very important in the context of biophysical
and float, into the upper layers of the water column as a dis- modeling, very few sensing platforms measure ocean cur-
persal strategy (Paris and Cowen 2004; Martinez-Quintana rents directly at any depth in the Mediterranean or elsewhere
et al. 2015; Ross et al. 2017). As a result, strong surface flow (Hayes et al., this volume), making characterisation of deep
in such regions is capable of consistently dispersing propa- water circulation difficult, especially for ocean models such
gules great distances (Johnston and Purkis 2015; Ross et al. as HyCOM, MFS, and NEMOMED12 that aim to emulate
2017). Conversely, in regions such as the tropical eastern Mediterranean and global deep-sea environments. Sea level
Pacific and closed ocean basins/gulfs such as the anomaly from satellite altimeters is often used to estimate
Mediterranean Sea and Persian Gulf, surface water flow is surface and approximate deep water flow, but stratification
generally much weaker and sometimes seasonal or influ- makes this method unreliable at best and is most suitable for
enced by meteorology (Pinardi and Masetti 2000; Estournel measuring surface water characteristics. Nevertheless, data
et al. 2003; Hayes et al., this volume). In the latter case, dis- assimilated ocean models are gaining traction that integrate
persal of larvae may be more radial or gradual, such as dem- in situ data such as CTD profiles and satellite-derived surface
onstrated by Andrello et al. (2013) and Johnston and Purkis flow measurements to more accurately simulate ocean
(2014) in the Mediterranean and Johnston and Purkis (2016) dynamics in surface waters and the deep.
in the Hawaiian Islands.
In the deep intermediate waters of the Mediterranean 40.2.2.2 Habitat Suitability
Sea – i.e. where CWCs reside – water flow is largely driven Benthic substratum is an important driver of connectivity of
by thermohaline mixing and overturning circulation and is CWCs in that offspring must encounter a location suitable
generally weaker and more intermittent than at the surface, for recruitment concluding the PLD. For example, given a
except in locations near submarine canyons and cascades tropical reef broadcast spawning coral such as Acropora mil-
(Pinardi and Masetti 2000; Hayes et al., this volume). Bottom lepora, a planula that reaches competency is not able to
topography, such as seamounts and escarpments, and baro- recruit to aphotic benthos or to a location where the benthic
clinic eddies also influence the direction and speed of water composition is outside of their tolerances such as mud or silt
flow (Cherubin et al. 2000; Freiwald et al. 2009; Taviani (Jones et al. 2016; Ricardo et al. 2017). Mediterranean
et al. 2015), which can be significantly different, direction- CWCs, in contrast, are found at deep, aphotic depths and
ally than at the surface. Intermediate waters of the Levantine primarily live on steeply inclined submarine walls and
(Levantine Intermediate Water – LIW) spread through the escarpments beneath bedrock overhangs and secondarily on
Mediterranean at depths of 0–500 m in complex cyclonic subtly inclined shelves (Freiwald et al. 2009; Orejas et al.
and anticyclonic eddy fields (e.g. the Rhodes Gyre, the 2009; Gori et al. 2012; Chimienti et al., this volume). Often
Cyprus Eddy), with a general trend of cyclonic rotation in CWC colonies are found in the vicinity of canyons, troughs,
the eastern Mediterranean basin and anticyclonic in the west and shelf edges which deliver nutrients and plankton on cas-
ern Mediterranean basin (Hayes et al., this volume). Salty cading or upwelling LIW that bath the colonies (Thiem et al.
LIW exits through the Sicily Channel and balances the net 2006; Freiwald et al. 2009; D’Onghia et al. 2015).
inflow of lower salinity water into the Mediterranean from Microhabitats preferred by the corals include bedrock lithol-
the Atlantic through the Straights of Gibraltar. West of the ogies containing overhangs and fissures that dissect the bed-
Sicily Channel, some flow of LIW flanks the northern rock (Freiwald et al. 2009; Chimienti et al. this volume).
African coast, eventually leaving the Sea through the Planulae settling in such regions would likewise have a
straights of Gibraltar. To the north, mesoscale anti- and greater success as surviving to maturity than those that may
cyclonic eddies (e.g. Western and Eastern Algerian Gyres, recruit to abyssal plains, for example.
Algerian Eddies and Sardinian Eddies) and along-coast cur-
Similar to unsuitable benthic structure and aphotic depths, While likely physiologically tolerable, salinity gradients
low water temperatures limit the distribution of some fauna in the Mediterranean may physically restrict CWC larval
both at high latitudes and also perhaps at depth, though typi- exchange to outside of the basin. The Mediterranean is a
cally the latter limitation is due to attenuation of sunlight relatively salty sea with an average salinity of ~38 (Borghin
(e.g. photosynthetic corals). Important to consider is over- et al. 2014) due to its largely closed nature and high rates of
wintering, especially for shallow corals or deep CWCs such evaporation (Skliris, this volume). At the Sea’s connection
as L. pertusa whose larvae may migrate vertically and be with the Atlantic Ocean through the Straights of Gibraltar,
dispersed in surface waters (Strömberg and Larsson 2017). lower salinity water of the Atlantic (salinity of ~ 35) flows
As the Mediterranean Sea is a marginal environment given over higher-density Mediterranean water, resulting in a net
its high latitude, shallow and surface waters are colder in the influx of water (Bryden et al. 1994). This zone, known as the
winter than deep water (Millot 1999), the latter perhaps serv- Almeria-Oran front is thought to act as a barrier to gene flow
ing as refugia for some marine organisms. Marine species in the Mediterranean, driven by different water densities that
accustomed to warmer temperatures and that successfully extend deep into the water column (Catarino et al. 2017).
recruit to shallow Mediterranean waters in northerly lati- Furthermore, this net flow of surface water may prevent
tudes during summer months are likely ephemeral due to floating pelagic larvae such as those of L. pertusa from exit-
overwintering temperatures that drop below their thermal ing the Sea into the Atlantic and serve as a biogeographic
tolerances (Johnston and Purkis 2014; Jimenez, pers. com- barrier to CWCs. Such water flow would be an integral com-
munication). This may help limit the spread of some warm- ponent to include in any biophysical modeling effort in the
water Lessepsian migrants from the Red Sea, but is probably context of understanding CWC connectivity between the
not a limiting factor to those native biota that are accustomed Mediterranean basin and the Atlantic. In any case, a three-
to water temperature fluctuations, such as L. pertusa which is dimensional representation of ocean conditions is requisite
found at both high and low latitudes and whose larvae likely for modeling the dispersal of Mediterranean CWCs, given
encounter and tolerate a large range of temperatures. their variable position throughout the water column spanning
Interestingly and conversely, the Mediterranean seems to be larval through adult life stages.
a marginal environment for some deep CWCs because the
water may be too warm during some parts of the year. For
example, L. pertusa thrives in a thermal envelope of 4 to 40.3 Biophysical Modeling
13 °C (Rogers 1999; Freiwald 2002; Taviani et al. 2017) and
peak Mediterranean water temperatures at 300 m sometimes 40.3.1 Integrating the Physical
reach >15 °C (Palanques et al. 2006). Furthermore, it is
thought that warming climatic conditions at the start of the The physical construct of a biophysical model is primarily a
Holocene may have holistically increased the temperature virtual two- or three-dimensional model grid which repre-
the Mediterranean and subsequently promoted the recession sents a real-world study domain such as the Mediterranean
of all CWC species in the sea (McCulloch et al. 2010; see Sea. The domain is a matrix of grid cells where each cell
chapters of the Past section in this volume). represents a discrete physical area of the ocean, which may
Salinity is not typically a physiologically limiting factor be of fixed or variable dimensions across the grid, and is
in the dispersal of marine organisms, aside from exceptional characterised by ocean conditions relevant to the species
locations where freshwater plumes may significantly lower being modeled. For Mediterranean CWCs, such data could
salinity to below marine levels or in estuarine environments comprise the speed and direction of water flow, salinity,
(Luiz et al. 2013). Such conditions in the Mediterranean ocean temperature, and bathymetry. The temporal and spatial
occur in limited locations such as the Rhone River delta and resolution of the grid is entirely dependent upon the data that
river discharges in the Adriatic, however freshwater inflows are used to parameterise the model. Often, nested grids of
are uncommon since the construction of the Aswan High different resolutions are used that reflect different temporal
Dam across the Nile River in the 1960s that reduced the and spatial resolutions of available ocean condition data.
inflow of freshwater into the Sea (Skliris this volume). Ocean forecast data from computer models such as the
Studies have also shown however that CWC larvae can toler- HYbrid Coordinate Ocean Model (HyCOM), Region Ocean
ate quite low salinities and readily cross pycnoclines Model System (ROMS), Nucleus for European Modelling of
(Strömberg and Larsson 2017) without increased mortality the Ocean (NEMO), Mediterranean Ocean Forecasting
of their planulae. It is unknown, however how an increas- System (MFS) are often used (e.g. Paris et al. 2013; Andrello
ingly saline Mediterranean may affect larval and adult mor- et al. 2013; Rossi et al. 2014; Johnston and Purkis 2016) to
tality of CWCs, though salinity fluctuations in the LIW layer characterise the model grid and are available at spatial reso-
throughout the basin strongly influence CWC growth lutions from <1 km to >100 km. The temporal resolution of
(Skliris, this volume). these ocean models ranges from hours to climactic averages
computed over years. Understandably, biophysical models to reflect biological or physical components outside of pas-
that use high resolution ocean data to parameterise the physi- sive particle transport (Liggins et al. 2013).
cal component are computationally expensive and therefore
parameters are chosen based on the science question that is
being asked. For example, some studies use very high resolu- 40.3.2 Two-Versus Three-Dimensional
tion data to analyse microscale processes such as inter-reef and Eulerian Versus Lagrangian
connectivity (e.g. Paris et al. 2013) and some models use
more broad resolution data to answer questions about con- Both two-dimensional and three-dimensional Eulerian and
nectivity over longer time periods and spatial spans (e.g. Lagrangian IBMs have been used in biophysical modeling
Andrello et al. 2013; Johnston and Purkis 2015). Also impor- studies within and outside of the Mediterranean (e.g. Cowen
tant is the consideration of strong land-ocean interaction, et al. 2000; Treml et al. 2008; Kool et al. 2010; Andrello
which is a characteristic of the Mediterranean Sea due to its et al. 2013; Hernandez et al. 2014; Johnston and Purkis
high temporal and spatial variability as a closed basin. 2015) and each method has strengths and weaknesses. Two-
The transport of marine particles, e.g. CWC larvae, in dimensional IBMs (e.g. Treml et al. 2008; Johnston and
Individual Based biophysical Models (i.e. IBMs, where indi- Purkis 2015) are usually faster computationally, easier to
vidual particles are tracked, as opposed to some Eulerian construct and arguable do an acceptable job of simulating the
models that simply track concentrations) typically can be dispersal of organisms whose larvae are typically constrained
binned into one of two fluid dynamics categories: Eulerian to the upper layers of the water column (i.e. due to buoyancy
models or Lagrangian models, referring the method that the and/or lack of vertical water flow), such as many coral larvae
larvae are transported within the model grid (Cowen et al. including, for part of their pelagic time, those of the CWC
2000; Zhang and Chen 2007). In an Eulerian IBM, larvae Lophelia pertusa (Treml et al. 2008; Johnston and Purkis
diffuse from cell-center to cell-center in a straight line and in 2015). Still, three-dimensional models are becoming more
a trajectory that reflects the velocity and direction of water commonplace as computing technology evolves (i.e. elimi-
flow of the source cell. The passive trajectories are some- nating the need for a super computer) and model algorithms
times modified by stochastic processes, such as planulae and ocean forecasts are refined. In the deep ocean where
swimming behavior, which are included in the model algo- CWCs reside, three-dimensional models are requisite as
rithm (e.g. Treml et al. 2008; Hernandez et al. 2014; Johnston deep ocean circulation does not intrinsically reflect surface
and Purkis 2015). This method is computationally swift and conditions and CWC larvae may either vertically migrate/
allows the production of simulations over long timespans. float (e.g. L. pertusa) or be neutrally or negatively buoyant
Larval trajectories in Eulerian IBMs generally mirror the transported within deep ocean currents.
time- and space-averaged direction and speed of water flow Speed and accuracy tradeoffs perhaps exist between
at somewhat lower resolution than a Lagrangian algorithm Eulerian and Lagrangian IBMs. Many times the end results
(Johnston and Purkis 2015). By contrast, in a Lagrangian are similar between the two model paradigms (e.g. Kool
model, larvae are transported through the model grid using et al. 2010 in contraposition to Johnston and Purkis 2015),
an algorithm which uses weighted averaging to diffuse the especially at large spatial and temporal scales. For broad-
larvae at discrete time-steps (e.g. 1 h) over the simulation scale studies, Eulerian IBM algorithms have a speed advan-
time period (e.g. Lett et al. 2008; Paris et al. 2013; Johnston tage over Lagrangian, despite their lower resolution, because
and Bernard 2017). The position of each larvae at each time- they integrate fewer parameters for the transport model,
step is corrected using either an iterative bi- or tri-linear which greatly optimises the model algorithm (Hernandez
interpolation equation (i.e. 2D versus 3D models, respec- et al. 2014). In contrast, high resolution Lagrangian IBMs
tively). Some Lagrangian models, especially those that are more accurately mimic the physics as they relate to larval
used to simulate high-resolution processes with fine spatial transport in water. In the end, the resolution compromises
or temporal resolution ocean condition inputs, use a Runge– inherent to each method must be decided upon given the spe-
Kutta 4th-order calculation which integrates a four-step cor- cific scientific question and available computing power
rection process to further refine larval diffusion at each (Liggins et al. 2013).
time-step (e.g. Paris et al. 2013). The Runge–Kutta method
increases computational overhead but may be desirable for
resolving fine-scale processes such as those occurring, for 40.3.3 Integrating the Biological
example, along deep ocean escarpments or mouths of can-
yons when modeling CWCs. Lagrangian and Eulerian IBMs Biophysical model algorithms integrate the biology of an
are widely accepted (though Lagrangian IBMs are becoming organism such as a CWC by assimilating the life history
more common) and robust simulations of particle movement characteristics over the model run timespan. For instance,
in a fluid and can integrate sub grid-scale processes intended many generic models use 30 days as a typical PLD for marine
larvae, tracking the origination, diffusion, and recruitment empirical abundance data for marine organisms are many
positions of larvae (e.g. Kool et al. 2010; Paris et al. 2013). times severely lacking, models make assumptions about
Most biophysical models include stochasticity to more real- population size or simply use a fixed population size at spe-
istically integrate sub-grid scale processes that are not other- cific locations throughout the model grid. The simulations
wise resolved by the model algorithm and also the random are then initiated using an estimated larval emission rate
nature of animal movements (e.g. Guizien et al. 2006; Paris based on the chosen population size (e.g. Johnston et al.
et al. 2013; Johnston and Purkis 2015). These random pro- 2017). In such cases, source/sink probabilities cannot be
cesses may represent micro-eddy diffusion or active migra- interpolated to natural abundance and should normally be
tion by the larvae, the latter of which is poorly understood for interpreted as potential source (sometimes reported as
most marine larvae including CWCs. Some models try to exporters) and sink (sometimes reported as importers) ratios
mimic diel migrations of larvae and also ‘sensory zones’, the given the starting conditions of the model and physical char-
latter where larvae are capable of actively seeking substrate acteristics of the synthetic model domain.
when passing within a certain distance of suitable habitat Often useful for illustrating transfer probabilities between
such as a reef tract or deep water escarpment (e.g. Kool et al. release and settlement sites are transition or connectivity
2010; Paris et al. 2013; Johnston and Purkis 2015). As these matrices. Transition matrices are valuable data visualisation
processes are largely untested in situ, care must be taken to tools to help interpret the spatial connectivity of a population
sensitivity test such integrated sub processes so that error is as the connections between sources and sinks and simply
not unintentionally introduced to the algorithm. graphed on an X/Y plot (Fig. 40.2). Each location within the
A small subset of biophysical models integrate post- study domain – i.e. a tangible, real world location – is repre-
recruitment processes such as adult mortality, maturity, and sented by a corresponding position on both the X and Y axes.
subsequent reproduction at maturity of successful recruits In the case of IBMs, individual settlement positions are plot-
(e.g. Johnston and Bernard 2017). These ‘generational’ bio- ted. Alternately, the recruitment positions can be summed
physical models are a further attempt to recreate the natural and represented as relative densities that are color-coded
process and may have utility in forecasting population struc- transfer probabilities that lie on the center diagonal represent
ture over many years or decades, especially in long-lived self-recruitment – i.e. the source and sink locations are iden-
species such as CWCs. The outputs of these models can be tical or within the same general area. The farther away the
compared to more traditional and literature-accepted biolog- positions plot from the diagonal, the greater distance larvae
ical connectivity measures such as genetic population struc- are transported away from the source population on most
ture. Prudence is appropriate when interpreting the results of matrices. Transition matrices are a standardised way of illus-
such models however as empirical abundance data is usually trating biological connectivity from biophysical models and
not available for many model species. Forecasted densities can be scaled to any spatial domain.
and connections between regions thus should be perceived as
potential metrics given ocean conditions and model condi-
tioning parameters (i.e. population size, locations, etc.). Still, 40.3.5 Limitations of Biophysical Models
generational models have advantages in that emergent popu-
lation structure can be measured over long temporal scopes. Biophysical models are inherently restricted by a paucity of
empirically-derived life history traits for many modeled spe-
cies included CWCs. As such, life history data are often sub-
40.3.4 Biophysical Model Products stituted with similar data from a congener or generic species
(e.g, Kool et al. 2010; Cardona et al. 2016; Johnston et al.
Given that individual larvae are usually tracked from spawn 2017). This situation adds an error factor that can be miti-
until recruitment in IBMs, it is possible to quantify not only gated by sensitivity testing the biological parameters (Treml
the connections between release sites and settlement sites, et al. 2012). Likewise, life history traits, even if measured
but also the interim and along-path trajectories, for example, empirically, are gradients and so sensitivity testing is also
of individual CWC larvae. These spatial-temporal data are prudent in such cases to establish the likely biological enve-
useful to quantify diffusion probabilities of the particles over lope that may be witnessed in situ by the model species. The
space and time and can be illustrated with larval diffusion same is true for integrating larval behavior and homing
maps and kernel density heat maps (Fig. 40.1). Both types of instincts. Much of the science on these components is in
maps are useful to visually interpret and quantify spatial pat- infancy. Data are not well verified with empirical studies to a
terns of larvae over the simulation time period. As the sources species level and therefore may not be applicable to marine
and sinks of propagules are also recorded, kernel density organisms with a passive dispersal strategy, or those that pre-
plots can also be used to illustrate source versus sink proba- sumably float in surface waters for a majority of the PLD
bilities (sometimes referred to as densities). As precise (Treml et al. 2008). Understandably, much care must be
Fig. 40.1 Example diffusion

and recruitment pattern (a) of
the benthic brooding coral
Tubastrea micrantha on oil
platforms in the Gulf of
Mexico. Larval diffusion
paths are color-colored from
cool (blue) to hot (red)
spanning the PLD of 14 days.
Recruitment positions noted
by black dots. Heat map (b)
demonstrating larval dispersal
densities, color coded from
blue (low) to red (high).
Recruitment positions are
black dots (© Matthew
Johnston 2018)
Fig. 40.2 Sample Transition

Matrix. Transition matrix
illustrating connectivity
between 12 regions. Source
locations are on the x-axis
and sink locations are on the
y-axis. Square symbols relay
locations of larvae that
successfully recruit. Squares
near the red diagonal line
indicate self-recruitment.
Circled in pink are two
locations (regions 1 and 2)
with high connectivity to
other locations. Circled in
yellow is a location with high
self-recruitment (region 10).
(© Matthew Johnston 2018)
given to explain the caveats of including larval behaviors biological dimensions. As such, field data that can be used to
until empirical evidence suggests otherwise. parameterise models are a necessity going forward.
The physical conditions used to parameterise models are Perhaps the weakest link when parameterising biophysi-
also not typically measured in situ, with the exception of cal models is a paucity of studies that accurately document
bathymetry data which has been historically measured quite biological drivers of connectivity such as PLD, natural mor-
accurately with acoustics and does not change appreciably tality, population sizes, and larval movements of marine
over time. Contemporaneous in situ measurements are not organisms. For deep-sea organisms such as CWCs, such
typically used for ocean currents and sea surface temperature information is particularly challenging to obtain and only
when modeling because ultra-high resolution, empirical available for a few species (Davies and Guinotte 2011;
measurements are simply not available at the spatial and Hilário et al. 2015). Ongoing work to quantify the length of
temporal scale needed. Most biophysical modelers therefore PLD, mortality rates, and also movements of planktonic lar-
rely on ocean hindcast models that assimilate data from sat- vae is of particular importance (Treml et al. 2008).
ellite imagery, drifters, and stationary buoys to supplement Additionally, very few biophysical models integrate a com-
the model algorithm (i.e. it is an ‘assimilated’ model). prehensive suite of post-settlement demographics, including
HyCOM is one of the most utilised global ocean condition active movement of adults and anthropogenic-induced mor-
models (in the Mediterranean NEMO-MFS and tality (Hernandez et al. 2014). Integration of such demo-
NEMOMED12 are commonly used) by biophysical model- graphics can provide a clearer picture of overall population
ers and the forecasts produced by HyCOM typically mimic structure over time.
real-world conditions to a high level of certainty, especially In addition to a lack of empirically-derived data on life
large scale ocean processes and surface waters. Indeed, history traits of model species, there is a challenge yet to be
cross-validation of HyCOM outputs against in situ measure- addressed when modeling organisms such as CWCs in the
ments has shown good correspondence on both a seasonal deep layers of the ocean. This is because oceanographic
and annual scales (Kourafalou et al. 2009). Still, HyCOM models such as HyCOM produce estimates (i.e. not real
data are estimates and as such, introduce another level of measurements) of water flow, salinity, and temperature and
complexity and error into biophysical model forecasts while they generally perform well in surface waters, they are
(HyCOM data are available freely to the public at www. largely untested in the deep ocean. Limitations of these esti-
hycom.org). mates impose a challenge enough in the surface layers and
Beyond parameterisation errors, inaccuracies can be are an acknowledged caveat of using model instead of in situ
introduced inadvertently into model algorithms by simple data. This challenge is exacerbated in the deep oceans simply
human error, which may negatively affect the output pro- because not enough is known about their dynamics and it is
duced by the model. Mitigation of these types of systemic difficult and costly to obtain in situ measurements of the
errors can be reduced and avoided by having multiple indi- deep ocean which may be then used to tune ocean models
viduals review the algorithm logic and computer code, using such as HyCOM. Still, progress is being made by the author
sensitivity analysis, and stress testing the model. Still, and others to validate and make recommendations on how
implicit error must be acknowledged as one of the limita- ocean models such as HyCOM compare to in situ data in an
tions of aiming to synthetically reproduce a sea-scape such effort to help them more realistically emulate the deep ocean
as the Mediterranean Sea within the confines of a virtual, environment. In conclusion, accurate physical and biological
computerised domain. components are critical to properly condition biophysical
models and are areas of future research that are in continued
need to advance the science of biophysical modeling in both
40.3.6 The Future of Biophysical Modeling the surface and deep layers of the World’s oceans, both of
which likely are influential environments for Mediterranean
Empirically-measured physical and biological phenomenon CWCs.
and ocean model forecasts continue to improve in spatial and
temporal resolution. Accordingly, the biophysical models
that ingest these data continue to progress in resolution. References
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Drop Chapter
The Interface Between Tectonic 41
Evolution and Cold-Water Coral
Dynamics in the Mediterranean
Rinus Wortel and Paul Meijer
Abstract Introduction
Circulation and water properties in the Mediterranean
basin, and thus the living conditions for marine biota, We analyse elements of the geodynamics (or, equivalently:
including cold-water corals, are a strong function of the tectonics) of the Mediterranean region envisaged to be rele-
connectivity of the basin with neighbouring water masses. vant to the dynamics of cold-water corals (CWCs) and their
The configuration of the basin and its connections with habitats. Some tectonic effects appear to be direct geosphere-
adjacent basins are governed by the interplay of large biosphere connections (in particular, the formation of faults
scale and regional scale geodynamical (or tectonic) pro- scarps as possible habitats, in combination with fluid seeps
cesses within the Mediterranean region. As to surface providing nutrients), whereas others are indirect, with the
area, it appears that the Mediterranean basin as a whole is geosphere-hydrosphere interactions affecting the circulation
closing whereas some of its sub-basins are opening, at the and marine conditions of the Mediterranean Sea.
expense of the eastern Mediterranean basin. More impor- The Mediterranean Sea is a marginal basin to the Atlantic
tant are opening or closure of gateway connections. The Ocean (e.g., Fusco et al. 2008; Lionello et al. 2012), which
pertinent Mediterranean gateways to the Atlantic Ocean implies relevant differences of marine conditions, in particu-
and the Black Sea are potentially subject to minor changes lar salinity and temperature, between these two basins. In
resulting from tectonics. However, the impact of such light of the future evolution of CWC habitats, the principal
possible changes on marine conditions, including those question to address concerns the nature and stability of the
for cold-water corals, would be slow and of minor magni- Gibraltar Strait which represents the gateway connection
tude compared to the effects of climate change. Typical between the two basins, and largely controls water masses
aspects of cold-water coral occurrences in the interchanges. Thus: Is the Mediterranean Basin opening or
Mediterranean region, notably the uplift and outcrops of closing? Whereas relative motion of the large Eurasian and
Plio-Pleistocene communities and the presence of steep African plates (a slow convergence) primarily seems to con-
faults (with steered fluid seeps providing nutrients) as trol the future of the Mediterranean Sea, we will argue that
preferred production areas, are accounted for by vertical tectonic processes within the Mediterranean Basin are likely
motions in subduction zone evolution. to be of more importance.
Keywords
Mediterranean Sea · Cold-water corals · Tectonics · Geodynamics of the Mediterranean Region
Gateways · Marine conditions
frica-Eurasia Convergence and Continental
A
Collision
As its name indicates, the Mediterranean Sea is surrounded

by land, or continents. It acquired this so-called landlocked
R. Wortel (*) · P. Meijer
Department of Earth Sciences, Utrecht University, basin configuration as a result of the relative motion of the
Utrecht, The Netherlands African and Eurasian plates, which in turn is part of the
e-mail: [email protected] global pattern of relative plate motions as described in plate

https://doi.org/10.1007/978-3-319-91608-8_41
500 R. Wortel and P. Meijer
Fig. 41.1 Active tectonics of the Mediterranean. Epicentres of shallow Inset: Schematic cross-section of the plate contact region in a subduc-
earthquakes (1992–2016, magnitude >4, NEIC catalogue) outline the tion zone. In a subduction zone one plate is subducted (underthrust)
often diffuse southern boundary of Eurasia. Arrows give motions with below another plate. The ocean-floor at the site of downwarping is
respect to Eurasia; rates in mm/year (Reilinger and McClusky, 2011; often marked by a deep-sea trench (which may, however, be filled by
Nocquet 2012). Discrete faults mentioned in the text are shown in sediments). In case of low relative convergence velocities of the plates
green. Key: Adr Adriatic Sea, Aeg Aegean Sea, AP Alghero-Provençal (less than a few cm/yr) the gravitational forces acting on the cold and,
basin, CA Calabrian Arc, Cor Corsica, Dard Dardanelles, DSF Dead hence, dense subducting plate (“slab”) lead to vertical sinking of the
Sea Fault, GA Gibraltar Arc, HA Hellenic Arc, NAF North Anatolian slab (indicated by vertical arrow), from the solid line geometry towards
Fault, RS Red Sea, Sar Sardinia, Sic Sicily, SM Sea of Marmara, Tyr the dashed line geometry. This is accompanied by horizontal motion of
Tyrrhenian Sea the trench or hinge zone at the surface (“roll-back”, indicated by hori-
Three sites of active or recent subduction (GA, CA, HA) are indicated zontal arrow, also referred to as “trench migration” or “arc migra-
by the red lines in the main figure. The triangles (dents) along these tion”), in the direction opposite to that of underthrusting. The
lines indicate the direction of underthrusting, i.e. the dip direction of the lithosphere above the subducted slab and behind the arc adjacent to the
subducted slab (see inset). plate contact (cf. the Hellenic, Calabrian and Gibraltar Arcs) is
Hexagons indicate living occurrences of framework-forming cold- extended (“back-arc extension”, towards the dashed line geometry),
water corals Lophelia pertusa and Madrepora oculata (compiled from leading to subsidence of the Earth surface or seafloor. (© Faculty of
Fink et al. 2015, and Taviani et al. 2017). Geosciences, Utrecht University)
tectonics. The lithosphere is the outer rather strong shell of at a spreading centre similar to the present-day Mid-Atlantic
the Earth, with a thickness characteristically in the order of Ridge. Relative to oceanic lithosphere, continental litho-
100 km. The lithosphere of the Earth is divided in a few tens sphere, in particular its upper crustal part, is made up of dif-
of large and somewhat smaller units: the “plates”. Since ferent rocks, with a lower average density. This tends to
about 80 Ma (i.e., 80 million years ago), the large litho- hamper the downward motion of subduction when – after an
spheric plates Eurasia and Africa, the latter encompassing episode of oceanic lithosphere subduction – continental lith-
Arabia until approximately 20 Ma, have been converging in osphere approaches and enters the trench of a subduction
an approximately NNW-SSE direction (Fig. 41.1; see zone at the margin of a continent, resulting in continental
Nocquet 2012 for an overview). The oceanic areas between collision, which eventually leaves an imprint in the geologi-
these continents – collectively referred to as Tethys Oceans – cal structure in the form of a usually complex mountain belt,
gradually decreased in size through the subduction (see the suture zone. The continuing motion of Africa and Eurasia
Fig. 41.1, inset) of the Tethys lithosphere in a complex sub- led to such a process in the region of present-day southeast-
duction (trench) system along the southern margins of ern Turkey-northern Iran-Irak (in the Bitlis and Zagros suture
Eurasia. zone; Fig. 41.1), in the Oligo-Miocene (from ~30 Ma to
To first order, the subducted lithosphere was oceanic in ~20 Ma; Okay et al. 2010). This was followed by opening of
nature, i.e. the lithosphere was formed by seafloor spreading, the Red Sea and formation of the Dead Sea Fault, giving rise
41 Tectonic Evolution and Cold-Water Coral Dynamics in the Mediterranean 501
to the splitting-off of Arabia from the African plate, to form the sense of “with/without subduction zones and related geo-
a new separate plate, the Arabian plate. In terms of the under- dynamic activity”). Their usual expression is that of a faulted
lying oceanic lithospheric basement, the present-day eastern slope with variable gradient, from the coastal region to the
Mediterranean (east of Sicily) is a remnant of the nearly deep parts of the basin, possibly with canyon-type of
completely lost Tethys Oceans. features.
Continental collision does not immediately lead to com- After considerable activity in the Neogene, with (horizon-
plete closure of all connections between adjacent marine tal) velocities of up to ~ 6 cm/year (Faccenna et al. 2001), arc
realms; a moderate-depth or shallow connection may remain migration and back-arc extension in the central Mediterranean
open for several million years. In case of the Arabia-Eurasia virtually came to an end at ~0.8–0.5 Ma (Goes et al. 2004);
collision, the closure of the Mediterranean-Indian Ocean the current (GPS) motion of the Calabrian Arc, the last active
gateway, at least as a deep marine connection, was probably segment in this region, relative to stable Eurasia is less than
completed in the Early Tortonian (Miocene), at about 11 Ma 5 mm/year in a NNE direction (Nocquet 2012).
(Hüsing et al. 2009). This left the Mediterranean basin with a Gutscher et al. (2012) have explored the recent tectonic
(composite) gateway to the Atlantic in the west and with con- activity of the Gibraltar Arc region, in the westernmost
nections to the Paratethys – an assemblage of predominantly Mediterranean; they concluded that very slow, ongoing sub-
shallow seas in central and eastern Europe – to the north of it duction most likely is the underlying process. Also, GPS data
(e.g., Palcu et al. 2015). Of the latter connections, the one to testify to the active motion (~5–6 mm/year, relative to Iberia
the Black Sea, through the Dardanelles/Sea of Marmara/ and Africa) of the arc region (Nocquet 2012). The Strait of
Bosphorus (Fig. 41.1), is the only one existing at present. Gibraltar gateway has known stages with a distinctly
restricted connectivity, which gave rise to the Messinian
Salinity Crisis (Flecker et al. 2015; Freiwald, this volume).
Internal Mediterranean Tectonics This “internal” roll-back process in the western-central
Mediterranean thus developed into a final stage in which
After continental collision between Africa/Arabia and only two relatively narrow slab segments, the east dipping
Eurasia in the Oligo-Miocene, the convergence velocity of Gibraltar arc segment and the WNW dipping Calabrian arc
the two plates decreased by approximately 50%, to the cur- segment (Fig. 41.1), continued to migrate to the west and
rent low values indicated in Fig. 41.1. In that situation, the east-southeast, respectively (Jolivet and Faccenna 2000;
downward directed gravitational forces acting on the sub- Wortel and Spakman 2000; Spakman and Wortel 2004). Of
ducted slabs along the northern boundary of the African plate these two, the Gibraltar segment is particularly relevant for
led to roll-back (see Fig. 41.1, inset), the oceanward migra- assessing future developments in the circulation and marine
tion of the subduction zones and their trench systems (Jolivet conditions of the Mediterranean, since it plays a key role in
and Faccenna 2000; Wortel and Spakman 2000). In the shaping the gateway to the Atlantic Ocean.
western-central Mediterranean the trench migration was in a The currently most active trench migration in the region
SE (later E-SE) direction, in the direction of the present-day occurs in the eastern Mediterranean, along the Hellenic Arc
Calabrian Arc, and also in W direction towards the present- (Fig. 41.1), at a velocity of about 30 mm/year. It is accompa-
day Gibraltar region (Fig. 41.1). It gave rise to the motion of nied by back-arc extension in the Aegean Sea, which, as yet,
Corsica, Sardinia and the Calabrian block away from Iberia has not reached the stage of oceanic lithosphere formation.
and (present-day) southern France, from about 30 Ma
onward. In the wake of the migrating slab segments, back-
arc extension occurred (Fig. 41.1, inset), resulting in subsid- Influence of Tectonics on Cold-Water Corals
ence (with velocities of less than 1 mm/year, but nevertheless
producing a total subsidence of 1 km or more over a period Direct Effects: Vertical Motions of the Ocean-
of a few million years), the formation of oceanic lithosphere Floor and the Formation of Fault Scarps
and the corresponding opening of the Algero-Provençal
basin between Iberia/Southern France and Corsica-Sardinia Two kinematic aspects of the subduction zone evolution in
(which stopped in the Langhian, about 15 Ma) and later the the Calabrian, Gibraltar and Hellenic Arcs are directly rele-
Tyrrhenian Sea. The back-arc extension process in the west- vant to the past and modern habitats of CWCs in the
ern Mediterranean is essentially identical, albeit of a smaller Mediterranean and to understanding that they are even
spatial scale, to the process of opening by seafloor spreading exposed on outcrops, a truly remarkable feature in the
of a large oceanic basin such as the Atlantic Ocean. The con- Mediterranean region (Taviani et al. 2005; Roberts et al.
tinental margins created by such extensional tectonic pro- 2009, pp 190–191):
cesses (seafloor spreading, rifting, back-arc extension) are (i) At the lateral edges of the migrating slab segments, the
named passive continental margins (active/passive used in roll-back process in the Mediterranean was accompanied by
near-vertical faulting (tearing) of the lithosphere (Govers motions, e.g., in rift zones and along the slopes of continen-
and Wortel 2005) in the Gibraltar area, a significant part of tal margins. This is evidenced in many CWC occurrences in
the coastal regions in the central Mediterranean (Tyrrhenian the Atlantic realm (e.g., Freiwald and Roberts 2005; Roberts
Sea-Sicily-Calabrian arc; Polonia et al. 2016), and in the et al. 2009) and – to a lesser extent – also in the Mediterranean
eastern part of the Hellenic Arc (Özbakir et al. 2013). (see Fig. 41.1), along the Spanish and French margins in the
Probably even the rifting in the Sicily Channel (Fig. 41.1) is N-NW part of the western Mediterranean, in the rift zone of
caused by the roll-back-process, in this case of the slab in the the Sicily Channel, off the South coast of Sardinia, and prob-
Calabrian arc (Argnani 2009). We propose that – as a direct ably also in the Adriatic Sea and the northern Aegean Sea
effect of tectonics – this may have produced the steeply (e.g., Taviani et al. 2017, this volume).
inclined fault scarps, steep bathymetry gradients and (hard) The above effects of tectonics on CWC dynamics are
substrates, apparently favourable as (although not necessary direct not only in a causal sense, but also spatially. They are
for) CWC growth habitats (Titschack and Freiwald 2005; localised at or near places where tectonic processes
Titschack et al. 2005; Roberts et al. 2009; Titschack, this vol- occur(red), and their spatial scale is local to regional. With
ume). Primary productivity being another governing factor respect to differences and similarities in CWC habitats
crucial for CWC distribution, the interplay between complex between the Atlantic Ocean and the Mediterranean Sea, we
seafloor bathymetry and water masses in highly productive note that extensional tectonic processes inherent to the for-
areas promotes suitable environmental conditions for CWC mation of passive continental margins (see Sect. Internal
habitats (e.g., White et al. 2005; Mienis et al. 2007; Tracey Mediterranean Tectonics) have been extremely prominent in
et al. 2011). the Atlantic Ocean (passive continental margins are often
(ii) The subduction zone background of the arcs implies termed “Atlantic margins”) where they form elongated belts,
that – even in case the horizontal convergence velocities are parallel to the strike of the continental margins. These are
very low (<10 mm/year) – vertical motions in the arc region readily identified in the distribution of CWC occurrences in
are possible, resulting from the evolution of the subducted the Atlantic Ocean (Roberts et al. 2009, pp 28–29, their
slab (Govers 2009). From the well-studied Calabrian Arc, it Figs. 2.3 and 2.5). In the smaller and more variable setting of
is known that uplift rates may reach values of about 1 mm/ the Mediterranean basin the passive margins are of more
year, with maxima of ~ 2.5 mm/year (Antonioli et al. 2006; restricted dimensions, and less dominant. Hence, in the
Faccenna et al. 2011). Such motions are neither an expres- CWC distribution in the Mediterranean both passive margins
sion of postglacial rebound nor of regional compression or and subduction zones (at active margins) play a role and,
collision (see Taviani et al. 2005); instead they are consid- jointly, contribute to a more irregular distribution pattern
ered to be intrinsic elements of the subduction process in a than in the Atlantic Ocean, even including surface exposure.
transient, terminal stage of activity, possibly including flow
of mantle material around slab edges (Faccenna et al. 2011)
and breaking-off and sinking of the deep part of a subducting I ndirect Effects: The Control of Tectonics
slab (Fig. 41.1, inset; Wortel and Spakman 2000). on Marine Conditions
The time scale at which Mediterranean CWCs are anal-
ysed, determines the perception of the impact of such verti- A widespread, basin-scale influence due to tectonics is pos-
cal motions. Also, the time scale of interest for future activity sible through tectonic control on the shape of the gateways.
may well differ from that for past activity. Whereas a 1 mm/ This represents an indirect effect of tectonics on CWCs:
year uplift rate during a period of 1–2 million years in recent Changes in gateway depth and width may critically affect the
geological history, resulting in a 1–2 km uplift, adequately connectivity between the basins involved and potentially
accounts for the remarkable outcrops of Plio-Pleistocene result in changes in the temperature, salinity, nutrient avail-
CWCs in the NE Sicily-Calabria region (Di Geronimo et al. ability and ventilation which are all thought to impact on
2005) and Rhodes (Titschack et al. 2005; Titschack and CWC development (Freiwald and Roberts 2005; Alvarez-
Freiwald 2005; Titschack, this volume), continuing uplift at Perez et al. 2005; Roberts et al. 2006; Fink et al. 2012, 2015;
the same rate integrated over a significantly shorter future see Smith et al. (2000) for a relationship proposed to use
period (say 1000 years) would produce a correspondingly CWC properties to infer paleotemperatures). The literature
small uplift of only 1 m. At present, finally, any tectonic-rate on the role of gateways is vast; in the context of the past cir-
uplift would incur only a minor effect on water depth because culation of the Mediterranean, see e.g. Rogerson et al. (2010,
sea level rises at a similar pace (Zerbini et al. 2017). 2012), Meijer (2012), Simon and Meijer (2015), de la Vara
It should be noted that hard substrates and steep bathymet al. (2015), de la Vara and Meijer (2016); for the present-
etry are not exclusively caused by tectonic activity in or near day Mediterranean, see also Hayes et al. (this volume) and
subduction zones; similar seafloor conditions can be the references therein. For the earlier Paratethys evolution this is
result of extensional tectonics accompanied by vertical a subject of active research (Palcu et al. 2015), aiming at
unravelling the Middle Miocene extinction of marine species cit of ~ 2.5 m are considered to be sufficient to generate a
in the central Paratethys (the eastern part, present-day magnitude ~ 7 earthquake. The time scale for possible long-
Romania). This prompts the question: Is the present gateway term changes, however, is governed by the long- term (hori-
configuration stable? To answer this question, we briefly zontal) relative motion along the North Anatolian Fault
explore the stability of the gateways (once) connecting the (about 23–25 mm/year; Nocquet 2012; Schmittbuhl et al.
Mediterranean Sea to the outside, in particular the now 2016).
closed one in the east (Bitlis), and the only now existing Both the Bosphorus and the Strait of Gibraltar provide the
gateway connection with the Paratethys, the Dardanelles/Sea Mediterranean Sea with an outlet for its relatively salty
of Marmara/Bosphorus gateway, or briefly, the Bosphorus waters and both act as a source (“inlet”) of water of lower
(Fig. 41.1). In the previous section, we already reviewed the salinity. Tectonically induced further constriction of these
subduction zone background of the Gibraltar Arc and the gateways would thus raise Mediterranean average salinity,
corresponding open gateway to the Atlantic, the Strait of and vice-versa. The Strait of Gibraltar also affects mean
Gibraltar, including its current horizontal and possible verti- water temperature in that it compensates the loss of heat
cal motions. incurred from the exchange of heat between the sea and the
atmosphere. Of the internal processes, perhaps the continu-
Eastern Gateway (Bitlis) Continental collision hampers ing migration of the Hellenic Arc may entail a small change
subduction but does not necessarily terminate it. If the forces in the deep circulation, given that the arc accommodates the
driving the converging plates can overcome the increased passage (east and west of Crete) of dense waters formed in
resistance, subduction continues albeit at an often signifi- the Aegean Sea.
cantly reduced rate. This appears to be the case for the Any tectonically induced change in marine conditions is
Africa-Eurasia motion: for the Bitlis suture zone, along the likely to be slow and best considered a long-term trend (100
Arabia-Eurasia plate boundary high resolution GPS mea- kyr to 1 Myr) overprinted by the higher frequency change
surements indicate a 15–20 mm/year motion of Arabia rela- due to, among others, orbital-induced climate variation
tive to Eurasia, in NNW direction (Reilinger and McClusky (Skliris this volume, discusses the current rise in salinity
2011). Thus, in this region the former gateway to the Indian related to changes in the water cycle). Of course, the very
Ocean is firmly closed and continuing plate motion will fact that the Mediterranean basin is sensitive to these cli-
maintain this condition. matic changes is due to its gateway-controlled landlocked
nature and thus, ultimately, a consequence of tectonics.
Bosphorus In contrast with the Gibraltar gateway, the

Bosphorus gateway to the Black Sea is not associated with a Conclusions
retreating slab segment in a subduction zone (roll-back). It
is, however, located near the active North Anatolian Fault The ongoing large-scale motion of the Eurasian and African
(NAF) and its extensions into the Sea of Marmara (Fig. 41.1). plates drives active and continuing closing (i.e., decrease of
Oktay et al. (2002) proposed that the present Bosphorus con- surface area) of the Mediterranean Sea basin as a whole.
nection resulted from the propagation of the NAF into the Within the Mediterranean basin, arc migration and back-arc
Sea of Marmara region; new rupturing of the right-lateral extension continue to lead to changing configurations of sub-
NAF in the Sea of Marmara region, with clockwise rotations basins, implying that the basins, notably the Aegean Sea and
of the two blocks on each side of the Bosphorus, was accom- possibly – to a very minor extent – the Tyrrhenian Sea, are
panied by left-lateral NNE trending faults affecting the area opening, i.e. increasing in size, at the expense of the Eastern
of the strait and the structure of the strait itself (“book shelf Mediterranean basin. More importantly than a reduction in
faulting”). surface dimensions of the Mediterranean Sea, tectonic pro-
cesses may lead to changes in the width and/or depth of the
In the past century, seismic activity along the NAF has Strait of the Gibraltar and Bosphorus gateways. The impact
been very considerable, with a distinct east-to-west migra- of such possible changes on marine conditions relevant for
tion, approaching the Istanbul area. In the context of possible CWCs, however, would be slow and of minor magnitude
further westward migration, recent analyses of seismicity compared to the effects of climate change.
and GPS observations led to the identification of a distinct Typical aspects of CWC occurrences in the Mediterranean
seismic gap (with a length of 30–45 km) in the fault seg- region, notably the presence of steep fault scarps (as preferred
ments in the central and eastern Sea of Marmara (Bohnhoff production areas) and the (long-term) uplift and surface expo-
et al. 2013; Ergintav et al. 2014; Schmittbuhl et al. 2016). sure of Plio-Pleistocene CWCs, are accounted for by faulting
The seismic gap is an indication of delayed earthquake activ- processes and vertical motions characteristic for the terminal
ity. The length of the gap and the estimated present slip defi- stage the Mediterranean subduction zones are in.
Acknowledgements The authors thank Claudio Lo Iacono, two anon- Govers R, Wortel MJR (2005) Lithosphere tearing at STEP faults:
ymous reviewers and the editors for their constructive comments, which response to edges of subduction zones. Earth Planet Sci Lett
improved the manuscript. 236:505–523
Gutscher MA, Dominguez S, Westbrook GK, et al (2012) The Gibraltar
subduction: a decade of new geophysical data. Tectonophysics
574-575:72–91
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Drop Chapter
The Mediterranean Is Getting Saltier: 42
From the Past to the Future
Nikolaos Skliris
Abstract
about 38.4 and 38.7 in the western and eastern subbasins,
The Mediterranean region is getting drier. Evaporation respectively). The density contrast between the highly saline
has been steadily increasing over the last few decades Mediterranean water and the relatively fresh Atlantic Water
driven by the rapid surface warming implying an increase (AW) drives an inverse estuarine circulation with
of latent heat loss from the sea surface. A long-term Mediterranean water of high salinity exiting through the bot-
decrease of river freshwater discharge has been also tom of the Gibraltar Strait into the Atlantic Ocean.
observed since the early 1960s, reflecting the impact of The high salt content plays a key role in mixing and dense
both river damming and recent climate change. As a result water formation processes. The Mediterranean has a very
of the net evaporation increasing rate, the salt content of active thermohaline (overturning) circulation (see Hayes
the basin has been also strongly increasing over the last et al., this volume) with very strong intermediate and deep
four to five decades with this salinification signal rapidly water formation in various sites of the basin (Fig. 42.1), and
travelling from the surface into the deep layers via the for this reason, it is often described as a laboratory model to
intense Mediterranean overturning circulation. Long-term study the global overturning circulation and to investigate its
increases were also observed in the salinity of the impacts on marine ecosystems and the earth’s climate sys-
Levantine Intermediate Water layer throughout the basin, tem (e.g. Malanotte-Rizzoli and Eremeev 1999). Northern
which strongly influences cold-water coral habitats and parts of the basin, such as the Gulf of Lions, the Adriatic Sea
distribution. Climate models predict that the present and the Aegean Sea, are characterised by continental very
warming and salinification trends will be accelerated over dry and cold winds during winter inducing strong cooling
this century and they are expected to have strong impacts and salting of the surface layer and thus increasing its den-
on marine ecosystems and biodiversity. sity, which, in combination with local intense cyclonic circu-
lation features strongly favour deep water formation. In
Keywords addition, the Levantine Intermediate Water (LIW) a very
Mediterranean Sea · Salinity · Water cycle · Evaporation · salty water mass formed through excessive evaporation in
River runoff · Cold-water corals the northeastern Levantine basin, spreading at intermediate
depths (200–600 m) throughout the whole basin, enhances
mixing and strongly preconditions the water column for deep
water formation (Hayes et al., this volume). The intensity of
The Mediterranean is a semi-enclosed strongly evaporative the overturning has major impacts on Mediterranean ecosys-
basin, i.e. evaporation exceeds precipitation and river runoff. tems as it controls deep-water renewal, oxygenation and
Therefore, it functions as a concentration basin which is nutrient replenishment of the upper layers. Moreover, LIW
evidenced from the transformation of the inflowing low strongly influences cold-water coral (CWC) habitats. The
salinity Atlantic surface waters (i.e. with a salinity of about CWC living grounds are usually found at depths ranging
36.2 at the Strait of Gibraltar) into very saline Mediterranean 350–600 m with maximum growth typically taking place
intermediate and deep waters (with a deep water salinity of close to the LIW core (Taviani et al. 2017; Chimienti et al.,
this volume; Hayes et al., this volume; Lo Iacono et al., this
N. Skliris (*) volume; Vertino et al., this volume).
Ocean and Earth Science, National Oceanography Centre, Another important feature of the Mediterranean is that it
University of Southampton, Southampton, UK is very sensitive to environmental and climate perturbations

https://doi.org/10.1007/978-3-319-91608-8_42
508 N. Skliris
Fig. 42.1 (a) Mediterranean 50

thermohaline circulation
N
45
a
g.
schematic prior to the Eastern
de
40
e,
Mediterranean Transient
tu d
a ti
(EMT) and (b) during the AW 35
L
EMT. Pathways of main water
30
masses including Atlantic LIW
Water (AW), Levantine 0
Intermediate Water (LIW), –1000
Depth, m
Eastern Mediterranean Deep –2000
WMDW
EMDW
Water (EMDW) and Western
–3000
Mediterranean Deep Water
(WMDW) are depicted. (From –4000
Tsimplis et al. 2006. ©
–10 –5 0 5 10 15 20 25 30 35
Elsevier)
Longitude, deg. E
50
b
.N
45
eg d
40
e, d
titu
AW 35
La
30
LIW
0
–1000
Depth, m
WMDW
–2000
EMDW
–3000
–4000
–10 –5 0 5 10 15 20 25 30 35
Longitude, deg. E
and it is considered to be a “hotspot” for climate change geological event that occurred around 6 million years ago,
(Giorgi 2006; Maier et al., this volume). Large industrial and the precursor of the Gibraltar Strait was closed, and the
population agglomerations surrounding the Mediterranean strong evaporative conditions in the absence of the fresh
Sea severely impact its marine ecosystems (Belkin 2009; Atlantic inflow dramatically increased salinity at levels not
Macias et al. 2014). The Mediterranean is a temperate tolerated by many organisms, including corals, strongly
transition region influenced by both the North African reducing biodiversity of the basin (Freiwald, this volume;
climate, characterised by warmer and drier conditions, and Wortel and Meijer, this volume). Large changes in the
the European climate, characterised by cooler and wetter Mediterranean hydrological properties also took place in the
conditions. In addition, due to its shape and limited exchange recent geological past with dire consequences for the CWC
with adjacent basins, changes in the surface heat and habitats (Taviani et al., this volume; Vertino et al., this
freshwater budgets cannot be compensated for by changes in volume). The Younger Dryas period (11,700–12,900 years
the exchange flows at the straits but mainly by changes in the ago) was the driest interval of the past 20,000 years (Kotthoff
hydrological properties of the basin (Bethoux and Gentilli et al. 2008) with almost glacial conditions and strong salting
1999), which in turn strongly affect its overturning circulation of the basin. On the contrary, the Holocene Climatic
and ecosystems (Skliris et al. 2007). Optimum (~6000–10,000 years ago) was a very warm and
In a steady-state balance of the salt budget, the salinity humid period for the Mediterranean region resulting in an
increase in the basin due to intense net evaporation intense freshening of the basin. The burial of the Tyrrhenian
(evaporation-precipitation-river runoff) is compensated for coral mounds under a thin veneer of silt, c. 11,000 years ago,
by net freshwater inputs at the straits connecting the seems to be related to increased continental runoff that
Mediterranean with the adjacent basins, i.e. the Gibraltar reached its maximum between 6000 and 9000 years ago
Strait and to a lesser extent the Dardanelles Straits (exchange (Remia and Taviani 2005). In particular, surface salinity was
with the Black Sea). However, in the geological past, the drastically reduced by four to seven below the present values
Mediterranean salt budget was far from being close to a in the Levantine Basin (Emeis et al. 2000). As a consequence
balance with drastic changes being observed in its of lighter surface waters, the overturning circulation and
thermohaline and ecosystem properties. Over the so-called deep-water renewal were considerably reduced. This in turn
Messinian Salinity Crisis (Krijgsman et al. 1999), a led to the development of deep-sea water anoxia with severe
42 The Mediterranean Is Getting Saltier: From the Past to the Future 509
implications for the Mediterranean ecosystems (Emeis et al. deep-sea shrimp (Cartes et al. 2011) as well as in sharks and
2000; Rohling et al. 2015). other top predators of the Mediterranean Sea (Cartes et al.
Before the 1990s, it was assumed that in the present era 2013).
the Mediterranean freshwater budget was close to a balance Atmospheric model reanalysis products, based on the
with small variations in the salt content of the basin. However, assimilation of various observational data, also show a strong
recent research demonstrated that the Mediterranean is increase in net evaporation over the Mediterranean Sea
getting saltier following the rapid warming over the last few surface over the last few decades (Mariotti et al. 2015),
decades. For example, thermodynamics indicate that the largely exceeding estimations of global water cycle
global water cycle is amplifying in a warming climate with amplification. This finding is also supported by coupled
dry regions getting drier and wet regions getting wetter (Held climate model historical simulations, although the obtained
and Soden 2006). Although changes in evaporation and evaporation increases are much less pronounced as compared
precipitation are very hard to measure (Hegerl et al. 2015), to atmospheric reanalyses and observations (Mariotti et al.
recent droughts in the Mediterranean region have been 2015).
already associated with anthropogenically forced drying With the global ocean receiving about 80% of surface
trends (Kelley et al. 2012). The last drought in the Levant freshwater fluxes, the three-dimensional ocean salinity field
(1998–2012) was probably the driest in the 900-year record is considered to be an integrator of changes in the global
(Cook et al. 2016). Observational studies indicate a water cycle. In contrast with air-sea freshwater fluxes,
continuous increase in evaporation over the Mediterranean salinity is a well-measured parameter, especially over the
Sea driven by the rapid surface warming during the last three last few decades. Surface salinity observations clearly
to four decades implying an increase of latent heat loss from indicate that precipitation-dominated oceanic regions such
the sea surface (Mariotti 2010; Romanou et al. 2010; Skliris as the tropical and subpolar regions are getting less saline
et al. 2012, 2018). and evaporation-dominated oceanic regions such as the
A large decrease in precipitation has also been observed subtropical gyres and evaporative marginal seas, such as the
over the second half of the twentieth century (Krahman and Mediterranean, are getting saltier (Durack and Wijffels 2010;
Schott 1998; Tsimplis and Josey 2001). However, the Skliris et al. 2014). Recent studies inferring water cycle
precipitation rate over the Mediterranean is also controlled changes from salinity observations indicate a global water
by natural variability related to the northern hemisphere cycle amplification ranging 2–4% over the last 50–60 years
atmospheric circulation that is mainly expressed by the (Durack et al. 2012; Skliris et al. 2014, 2016). Salinity-
so-called North Atlantic Oscillation (NAO) (Hurrell 1995). inferred net evaporation increase is estimated to be much
The long-term increase of the NAO index from the late 1960s larger over the Mediterranean Sea at 8–12% over 1950–2010
to the mid-1990s was suggested to be a key factor contributing (Skliris et al. 2018).
to the reduced precipitation over the Mediterranean Sea Together with warming, coherent and robust trends of
during this period (Krahman and Schott 1998; Tsimplis and increased salinity are evidenced in key Mediterranean water
Josey 2001). masses since the 1950s, consistent with the strong net
A long-term decrease of freshwater input in the evaporation increase (Rohling and Bryden 1992; Krahman
Mediterranean is associated with decreasing river freshwater and Schott 1998; Bethoux and Gentili 1999; Rixen et al.
discharge, reflecting the impact of both river damming and 2005; Vargas-Yanez et al. 2010; Borghini et al. 2014;
recent climate change. A decrease larger than 50% in the Schroeder et al. 2016). The deep waters of the western basin
freshwater discharge of rivers feeding directly or indirectly have become saltier for at least the past 40 years at rates of
(i.e. the Black Sea rivers through the Dardanelles inflow) the about 0.015 per decade (Borghini et al. 2014). Below 1000 m
Mediterranean Sea was estimated since the second half of depth, the Mediterranean basin exhibited the strongest
the nineteenth century due to damming (Poulos and salinity gain in the World Ocean since 1950 (Skliris et al.
Drakopoulos 2001). Ludwig et al. (2009) estimated a 2014). Long-term increasing trends in the LIW core salinity
reduction in the river freshwater discharge in the are also reported throughout the basin (Rohling and Bryden
Mediterranean basin of at least 20% between 1960 and 2000. 1992; Skliris and Lascaratos 2004; Borghini et al. 2014).
After the construction of the Aswan Dam in the early 1960s, Salinity increases at intermediate layers were partially
the Nile river runoff was drastically reduced affecting the salt attributed to the Nile outflow drastic reduction after the mid-
budget and the thermohaline circulation of the whole basin 1960s when induced an enhanced salt preconditioning for
for several decades (Rohling and Bryden 1992; Skliris and LIW formation and a large increase in the salinity of the
Lascaratos 2004; Skliris et al. 2007). Although the effects of newly formed intermediate waters (Skliris and Lascaratos
these thermohaline circulation changes on deepwater corals 2004; Skliris et al. 2007). The LIW circulation spread this
are still unknown, negative consequences are reported for salinification signal westward and through the Sicily Strait
deep marine ecosystems, such as the drop in abundance of into the western Mediterranean basin (Hayes et al., this
510 N. Skliris
Fig. 42.2 (a) Volume-

averaged salinity anomaly
annual time series over
1970–2015 for the Western
Mediterranean (WMED, blue
lines) and Eastern
Mediterranean (EMED, red
lines) subbasins and for the
350–600 m layer and (b) the
2000 m - bottom layer.
Salinity data are derived from
the Enhanced Ocean Data
Assimilation and Climate
prediction (ENACT) archive
version 4 (EN4, subversion
En4.1.1, http://www.
metoffice.gov.uk/hadobs/en4)
objectively analysed monthly
observational dataset. (Good
et al. 2013)
volume). These large changes in LIW formation rate, The long-term increased Mediterranean salinity signal is
hydrological properties and circulation are expected to affect also evidenced in the Mediterranean Outflow Water (MOW)
occurrence and distribution patterns of CWC habitats as well exiting into the Atlantic ocean, and it is clearly depicted at
as corals’ biology and physiology. The effects of hypersaline intermediate depths (1000–1500 m) in the subtropical
or hyposaline conditions on shallow-water corals are found Northeast Atlantic (Curry et al. 2003; Potter and Lozier
to be in general negative (e.g. Jokiel et al. 1993; Ferrier- 2004; Skliris et al. 2014). The MOW salty vein reaching the
Pagès et al. 1999; Kuanui et al. 2015) or positive in other northern Atlantic is a very important factor impacting deep
cnidarians where salinity interacts with other factors, such as water formation processes in the North Atlantic (Reid 1979;
temperature (Gegner et al. 2017). Salt content of the 350– McCartney and Mauritzen 2001). Hydrological observations
600 m layer, where maximum CWC growth is typically show that warming almost compensates for the salting effect
observed (Taviani et al. 2017), increased in both the eastern resulting in no significant change in density in MOW over
and western Mediterranean subbasins since the early 1970s the second half of the twentieth century (Potter and Lozier
at rates of about 0.02 per decade (Fig. 42.2). 2004). However, over the last 15 years, a strong density
The increasing salinity rate in the intermediate and deep increase is observed in the deep layer of the western
layers seems to be accelerated over recent extreme climate Mediterranean basin driven by the accelerated salinity
transient events (i.e. abrupt shifts of the “ocean climate” with increase (Borghini et al. 2014; Hayes et al., this volume). A
large changes in the thermohaline circulation and saltier and denser MOW may enhance deep water formation
hydrological properties, see Fig. 42.2), i.e. the Eastern in the northern North Atlantic with strong implications for
Mediterranean Transient (EMT) during the 1990s (e.g. Klein the global overturning circulation and subsequently for the
et al. 1999) and the Western Mediterranean Transient earth’s climate system and marine ecosystems. An
(WMT), which started in the mid-2000s (e.g. Schroeder intensification of the Atlantic meridional overturning
et al. 2016; Hayes et al., this volume). These abrupt salinity circulation (AMOC), partially driven by MOW after the
changes seem to be superimposed on the longer-term Younger Dryas 11,600 years ago, led to the fastest postglacial
quasilinear increases in salinity due to changes in surface CWC range expansion ever recorded (Henry et al. 2014).
freshwater fluxes associated with global warming and/or Coupled climate models predict excessive drying and
natural variability. Such climate transient events may be warming of the Mediterranean region during the twenty-first
more frequent and extreme in the future as the salinity of the century (Mariotti et al. 2008, 2015; Somot et al. 2008).
basin continues to increase inducing a more efficient salt Following the strong net evaporation increase, large salinity
preconditioning of the water column for deep water gains are predicted throughout the basin (Macias et al. 2015;
formation. Adloff et al. 2015; Maier et al., this volume). Regional
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oceanography, and the periodic development of anoxic events Hayes D, Schroeder K, Poulain PM, et al (this volume) Review of the
(sapropels). Earth Sci Rev 143:62–97. https://doi.org/10.1016/j. circulation and characteristics of intermediate water masses of the
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Drop Chapter
The Spread of Non-indigenous 43
Species in the Mediterranean – A Threat
to Cold-Water Corals?
Bella S. Galil
Abstract The spread of non-indigenous species (NIS) is one aspect of

Only few live records of cold-water corals are known global change and is considered to be among the main direct
from the Aegean and Levant seas, though antipatharians, drivers of biodiversity loss, affecting environmental and eco-
ceriantharians, zoantharians, gorgonians and pennatu- nomic damage. The negative effects of NIS are exacerbated
laceans have been recorded from their continental shelf by climate change, pollution, habitat loss and human-induced
and upper slope. These mesophotic coral communities, disturbance. The most harmful NIS displace native species,
including the Corallium rubrum (Linnaeus, 1758) colo- alter community structure and food webs, and change eco-
nies in Crete and southeast Turkey, are already within the system functioning. Non-indigenous species have trans-
depth range of disruptive carnivorous and omnivorous formed marine coastal habitats worldwide and their impact
non-indigenous species introduced though the Suez has been increasing inexorably (Millenium Ecosystem
Canal. The recent enlargement of the Suez Canal has Assessment 2005).
raised concern over increasing propagule pressure of Complex and fundamental alterations to the Mediterranean
deeper living species. In fact, the recently observed Sea, including increases in NIS, have affected the structure
“descent” of Erythraean non-indigenous species from the and functioning of the sea and the consequent provision of
upper to lower continental shelf and upper slope may be goods and services (Micheli et al. 2013; European
also a harbinger of temperature-dependent range expan- Environmental Agency 2015). The number of recorded
sion, both horizontal and vertical. As mesophotic coral metazoan NIS in the Mediterranean Sea (over 800) is far
communities in the easternmost Mediterranean have higher than in other European seas – nearly triple the number
barely been documented, it is impossible to predict the of records known from the western European margin – and it
possibility of degradation and loss of native populations, doubled between 1980 and 2016 (Galil et al. 2014). From
habitats and ecosystem services. However, preliminary those species, 470 were introduced through the Suez Canal
studies on impacts of the invasive Indo-Pacific lionfish on (Erythraean NIS), the balance were primarily introduced by
Caribbean mesophotic reef communities suggested a shift shipping and mariculture. The number and abundance of
in community structure. The spread of non-indigenous Erythraean NIS are substantially greater in the Levant where
species to mesophotic depths requires a concerted effort they are prominent in many coastal habitats (Steinitz 1970;
to map these habitats and study their communities. Por 1978; Galil 2007; Galil et al. 2014). Vectors determine
the choice of introduced taxa, their geographical origin and
Keywords propagule pressure: where the Suez Canal is the main vector,
Bathymetric range expansion · Mesophotic coral most NIS are of tropical Indo-Pacific origin and comprise
assemblages · Suez Canal · Ecological impact taxa actively spreading as adults or passively transported as
larvae; where vessels and aquaculture are the prevailing vec-
tors, the taxonomic composition and native ranges of NIS are
more diverse and depend on shipping routes and mariculture
transfers. As these activities were confined to the shallow
B. S. Galil (*)
shelf, it was assumed that so would the NIS. Indeed, until the
The Steinhardt Museum of Natural History, Tel Aviv University,
Tel Aviv, Israel millennium NIS records were largely limited to the coastal
e-mail: [email protected] zone. That was about to change.

https://doi.org/10.1007/978-3-319-91608-8_43
514 B. S. Galil
Recent findings of NIS populations established in deeper

waters have upended this paradigm – a growing number of
NIS have been collected on the deeper shelf, even beyond the
shelf break and well into the upper slope. The Erythraean
portunid crab Charybdis longicollis (Leene, 1938), recorded
in the Mediterranean since 1954, and its sacculinid parasite,
Heterosaccus dollfusi Boschma, 1960, were collected off
Israel as deep as 250 m (Innocenti et al. 2017). Off the
Mediterranean coast of Israel in 1960–1962 C. longicollis
was abundant at 36 m depth, but at a depth of 82 m “only
single specimens were taken” (Gilat 1964: 14, fig. 4). In the
late 1970s 3.5 times as many individuals were collected in
35 m as in 50 m, and only two specimens were collected in
80 m (Galil and Lewinsohn 1981). However, in recent sur-
veys (2008–2012) the highest numbers of specimens were Fig. 43.1 Gonioinfradens giardi (A. Milne Edwards, 1861), Rosh
collected between 40 and 80 m, but specimens were also col- HaNikra marine nature reserve, Israel, 2015. (Photographed by © Oren
lected also at 100, 120 and 250 m depth (Innocenti et al. Klein)
2017). The goldband goatfish Upeneus moluccensis (Bleeker,
1855) and the lessepsian lizardfish Saurida lessepsianus
Russell, Golani and Tikochinski, 2015, first recorded in the
Mediterranean in 1935 and 1952 respectively, constitute a
significant component of the local trawl fisheries and have
been common in trawls hauled from depths of 100 and 120 m
(Levitt 2012). Charybdis longicollis, U. moluccensis and S.
lessepsianus are widespread and abundant throughout the
eastern Mediterranean Sea, and the latter has spread west-
wards to Albania and Tunisia (Rakaj 1995; Ben Souissi et al.
2005). In 2004 the bathydemersal spiny blaasop Tylerius spi-
nosissimus (Regan, 1908) was collected off Rhodes at 90 m,
and again in 2009 in 50–80 m (Corsini et al. 2005, 2010a, b),
and in 2010 off Israel at 120–140 m (Golani et al. 2011). In
2010, specimens of the spotfin cardinal Apogon queketti
Gilchrist, 1903 were collected at depths of 140–150 m in the
gulf of Antalya, Turkey (Gökoğlu et al. 2011). In the same Fig. 43.2 Pterois miles (Bennett, 1828), Rosh HaNikra marine nature
year a portunid crab, Gonioinfradens giardi (Nobili, 1905), reserve, Israel, 2014. (Photographed by © Oren Klein)
was collected off Rodos Island on biogenic debris at 200 m
(Corsini-Foka et al. 2010a, b, as G. paucidentatus (A. Milne through-current velocities on propagule pressure of
Edwards, 1861) (Fig. 43.1). In 2010 and 2011, large numbers Erythraean NIS are all too clear – increasing the delivery of
of Randall’s threadfin bream Nemipterus randalli Russell multiple species and in particular deeper living ones. As the
1986 were collected at depths of 100 and 120 m off the sea is warming, the expansion of their bathymetric range
Israeli coastline (fig 5a in Stern et al. 2014,). Nuttal et al. may be accelerating. In fact, the recently observed “descent”
(2014) documented the occurrence of Pterois volitans of Erythraean NIS (references given above) from the upper
(Linnaeus, 1758) and P. miles (Bennett, 1828) to depth of to lower continental shelf and upper slope may be a harbin-
112 m in the northwestern Gulf of Mexico, with the greatest ger of temperature-dependent range expansion, both hori-
abundance between 80 and 90 m, whereas Lesser and Slattery zontal and vertical.
(2011) suggested a shift to algal dominated communities in With few exceptions, the ecological impact of NIS on the
Bahamian mesophotic reefs is associated with the invasion indigenous Mediterranean biota is poorly known (Zibrowius
of the Indo-Pacific lionfish. Pterois miles has been spreading 1992; Boudouresque 2004; Katsanevakis et al. 2014),
rapidly also in the Mediterranean Sea (Ounifi-Ben Amor although some species have caused major degradation and
et al. 2015; Azzuro et al. 2017) (Fig. 43.2). loss of native populations, habitats and ecosystem services
All these species have in common their mode of introduc- (Galil 2007). The individual and cumulative impacts of these
tion through the Suez Canal. The implications of the succes- species affect the conservation status of native species and
sive enlargements of the Suez Canal combined with higher critical habitats, as well as the structure and function of eco-
43 Non-indigenous Species in the Mediterranean. A Threat to Cold-Water Corals? 515
systems and the availability of natural resources. A century References

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Altuna and Poliseno, this volume; Chimienti et al., this vol- Galil BS (2007) Loss or gain? Invasive aliens and biodiversity in the
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Curr Opin Environ Sustain 7:118–126 scleractinian cold-water corals as a result of global climate change.
Smith C, Sakellariou D, McCoy F, et al (2009) Deep coral environ- A synthesis
ments south of Crete. 9ο Πανελλήνιο Συμπόσιο Ωκεανογραφίας & Movilla J (this volume) A case study: variability in the calcification
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Steinitz H (1970) A critical list of immigrants via the Suez Canal. Orejas C, Jiménez C, Gori A, et al (this volume) Corals of Aphrodite:
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Zoology, Hebrew University Jerusalem, pp 64–74 [mimeo]
Fate of Mediterranean Scleractinian
Cold-Water Corals as a Result of Global 44
Climate Change. A Synthesis
Cornelia Maier, Markus G. Weinbauer,
and Jean-Pierre Gattuso
Abstract Keywords
This chapter addresses the question as to how Mediterranean cold-water coral · Climate change · Ocean
Mediterranean cold-water corals might fare in the future acidification · Temperature · Calcification · Respiration
under anthropogenically-induced global climate change.
The focus on three most prominent scleractinian cold-
water corals species, the two branching and habitat-
forming forms Madrepora oculata, Lophelia pertusa and 44.1 Introduction
the solitary cup coral Desmophyllum dianthus. We pro-
vide an introduction to climate change principals, high- 44.1.1 Global Climate Change
light the current status of the marine environment with
regard to global climate change, and describe how climate Climate change refers to a change in weather conditions over
change impacts such as ocean acidification are predicted a longer period of time, taking place from decades to mil-
to affect key calcifiers such as scleractinian cold-water lions of years and usually referring to (regional) rise or fall of
corals in the Mediterranean region. A synthesis of the mean temperatures, changes in precipitation and parameters
experimental cold-water coral studies conducted to date such as the frequency of extreme weather events. Throughout
on climate change impacts: The present state of knowl- Earth’s history long-term climate change and climate events
edge reviewed in this chapter takes into account the num- have taken place as a consequence of internal or external
ber of experiments that have been carried out in the forcing of the naturally occurring climate system. The most
Mediterranean as well as for comparative purposes in recent, relatively short-term change in the global climate
other parts of the world, to examine the effects of climate however, has been more dramatic and due to anthropogeni-
change on the corals. We assess the statistical robustness cally produced greenhouse gases that have acted on the cli-
of these experiments and what challenges the presented mate system by reducing the heat radiation to space.
experiments. A comprehensive multi-study comparison is Anthropogenically induced global warming trend had
provided in order to inform on the present state of knowl- already been described in the late nineteenth century
edge, and knowledge gaps, in understanding the effects of (Arrhenius 1896). At that time, the contribution of industri-
global climate change on cold-water corals. Finally we ally produced CO2 was thought to have minor effects with
describe what the fate could be for the important sclerac- respect to the overall natural climate dynamics and it was
tinian coral group in the Mediterranean region. believed that the observed warming would at least be par-
tially beneficial to human prosperity: “…there is good mixed
with the evil. …, we may hope to enjoy ages with more equa-
C. Maier (*) · M. G. Weinbauer ble and better climates, especially as regards the colder
Sorbonne Université, CNRS, Laboratoire d’Océanographie de
regions of the earth…” (Arrhenius 1908). Since this time
Villefranche, Villefranche-sur-Mer, France
e-mail: [email protected] research to investigate climate change impacts has intensi-
fied and there is now strong evidence, that besides the
J.-P. Gattuso
Sorbonne Université, CNRS, Laboratoire d’Océanographie de increase in temperature, our global climate has become less
Villefranche, Villefranche-sur-Mer, France stable with more frequent and intense weather events due to
Institute for Sustainable Development and International Relations, the present day atmospheric levels of CO2 concentration
Sciences Po, Paris, France being higher than at any time during the last 2.6 million

https://doi.org/10.1007/978-3-319-91608-8_44
518 C. Maier et al.
years (Lewandowsky et al. 2016). Since pre-industrial times, Sabine et al. 2004; Landschützer et al. 2016). Since pre-
atmospheric CO2 increased from 280 to 400 ppm and a fur- industrial times about 25–30% of atmospheric CO2 has been
ther doubling is projected until the end of the century (IPCC absorbed by the oceans. The rising partial pressure of CO2
2013). This rate of change is unprecedented with a anthropo- (pCO2) has major consequences as CO2 reacts to carbonic
genic CO2 release rate being 14,000 times faster than the acid in solution resulting in the reduction of ocean pH termed
natural net release of CO2 (Zeebe et al. 2016). ocean acidification (OA). There is an increasing awareness
that climate change is altering the physical and biogeochemi-
cal status of the surface ocean and with the simultaneous
44.1.2 The Role of the Oceans increase of hydrogen and bicarbonate ions and a decrease in
carbonate ions the seawater pH will decline by an average
The oceans play an important role in global climate through 0.3 units by the end of the century (Caldeira and Wickett
gas and heat exchange and it is this thermal capacity of the 2003; Cicerone et al. 2004; Feely et al. 2004; Sabine et al.
oceans that moderates the climate and slows down global 2004; Orr et al. 2005b; Gattuso et al. 2015). This change also
warming. Heat exchange with the ocean affects the upper affects the calcium carbonate saturation state (Ω) in seawater
ocean layers more strongly than the deep ocean and up to which is the discriminant parameter with respect to the pre-
90% of the additional heat and about one third of anthropo- cipitation and solution of calcium carbonates. Solubility
genic CO2 released since pre-industrial times has been increases at higher pressure and lower temperature, which
absorbed by the oceans. Since the 1970s ocean temperatures means that Ω decreases with increasing water depths and at
too have increased by 0.11 °C per decade in the upper 75 m higher latitudes. OA has been postulated to be of a major con-
and by 0.015 °C at 700 m water depth (Levitus et al. 2012; cern for various calcifying organisms as they depend on the
Rhein et al. 2013). An apparent ‘hiatus’ in global warming surrounding seawater to build their shells or in the case of
and sea surface heat uptake during the last 15 years had been cold-water corals (CWCs), their skeletons (Orr et al. 2005a,
identified (IPCC 2013), while the deeper ocean has contrib- b; Kleypas et al. 2006). Over the last decade research on the
uted significantly to an additional and recent heat sequestra- effects of OA on marine organisms has intensified and new
tion. This factor explains the observed slowing down of priorities for future research identified. OA impacts have
atmospheric warming during the last decade (Hansen et al. highlighted the urgent need to study keystone species, eco-
2011; Meehl et al. 2011; Chen and Tung 2014; Cheng et al. system engineers and those ecosystems considered most vul-
2015; Yan et al. 2016; Desbruyères et al. 2016; Bova et al. nerable or most resilient to global climate change (Riebesell
2016), with recent research substantiating the ongoing ocean and Gattuso 2015). Like their tropical counterparts, sclerac-
warming trend (Kosaka and Xie 2013; Karl et al. 2015; tinian CWCs grow an aragonitic 3-D matrix like exoskeleton,
Lewandowsky et al. 2016; Fyfe et al. 2016; Song et al. 2016; and as such are susceptible to changes in the seawater carbon-
Hausfather et al. 2017). Global change not only affects the ate chemistry. The surface ocean is currently supersaturated
general heat content and warming of the oceans, but has in aragonite and calcite, the two forms of carbonate that
widespread consequences related to the temperature depen- marine calcifiers use to form their shells or skeletons. The
dent state of water as solid ice, liquid or vapour. Changes in ongoing absorption of atmospheric CO2 by the oceans results
sea level, salinity and freshwater content show strong regional in a shallowing of the aragonite saturation horizon (ASH), the
trends dependent on the ratio of evaporation, precipitation, critical depth between precipitation and dissolution of arago-
river discharge and melting of glaciers and ice caps (Church nitic calcium carbonate. Work by Feely et al. (2012) showed
et al. 2011; Pierce et al. 2012; Levermann et al. 2013; Rhein that the offset in the ASH in the South Pacific between the
et al. 2013). Since the 1950s the contrast between high- and 1990s and the 2000s had shifted by 10 m. In the New Zealand
low-salinity regions has increased by 0.13 (Rhein et al. 2013). region estimates suggest that the ASH may have already
These changes in seawater temperature and salinity affect the shoaled by an order of 50 to 100 m (Bostock et al. 2013,
density and volume of seawater causing changes to the steric 2015; Law et al. 2016). This places the deep-sea aragonitic
sea level (Antonov et al. 2002; Llovel et al. 2014), circulation scleractinian CWCs, being confined to the deep waters and to
of water masses and to ocean currents (Purkey and Johnson colder regions at great risk with 70% of the CWC habitats
2010; England et al. 2014; McGregor et al. 2014). becoming exposed to undersaturated conditions (Guinotte
et al. 2006; Mikaloff-Fletcher et al. 2006; Bostock et al.
2015). Scleractinian CWC ecosystems are thought to be one
44.1.3 Ocean Acidification of the most vulnerable groups that will be impacted by global
climate change. This factor and additional anthropogenic
Anthropogenic CO2 released to the atmosphere is partially stressors such as deep-sea trawling, mineral exploration, min-
taken up by the oceans and acts as a major net sink for anthro- ing, and marine pollution (Turley et al. 2007; Roberts et al.
pogenic carbon (Revelle and Suess 1957; Orr et al. 2001; 2016), add to the vulnerability of CWCs in a high CO2 world.
44 Mediterranean Scleractinian Cold-Water and Global Climate Change 519
44.1.4 Cold-Water Corals 44.1.5 Climate Change in the Mediterranean

Region
While the biology of shallow-water tropical corals and their
response to global change (warming and OA) has been The Mediterranean region has been identified as one among
studied for many decades, research on the biology and physi- the most important climate change Hot-Spots world-wide as
ology of deep-sea CWCs such as the abundant scleractinian it has become warmer and drier throughout the twenty-first
coral group is still in its infancy (but see Reynaud and century (Giorgi 2006). The variability in warming during
Ferrier-Pagès, this volume and references therein). Until a summer is twice the global standard deviation (Hansen and
decade ago knowledge was based on few studies providing Sato 2016). With this large increase in variability and a
some insights on skeletal extension (Bell and Smith 1999; decrease in mean precipitation during the dry, warm seasons
Mortensen 2001), food capture (Mortensen 2001), potential the Mediterranean constitutes one of the most responsive and
food sources (Kiriakoulakis et al. 2005; Duineveld et al. affected regions with respect to global change (Giorgi et al.
2007), the respiratory response to temperature change or 2001; Giorgi and Lionello 2008; Mariotti et al. 2008;
hypoxia (Dodds et al. 2007) and reproductive ecology Alessandri et al. 2014).
(Waller and Tyler 2005; Waller et al. 2005). However, the The Mediterranean Sea is nearly land-locked, connected
knowledge on the abundance and distribution of CWCs has to the Atlantic by the shallow (300 m) Strait of Gibraltar.
advanced rapidly since the 1990s due to several factors such Evaporation greatly exceeds precipitation which drives the
as an increase in deep-sea biodiversity surveys (e.g. thermohaline circulation with deep and intermediate dense
Zibrowius and Gili 1990; Rogers 1999; Roberts et al. 2009; water convection in several basins and a unique open upper
Buhl-Mortensen et al. 2010; Mastrototaro et al. 2010; thermohaline cell that acts in a similar way as the global con-
Tittensor et al. 2010; Gori et al. 2013; Smith and Williams veyer belt while it is characterised by a much shorter resi-
2015); access to more sophisticated deep-sea technology dence time of ca. 100 years (Malanotte-Rizzoli et al. 2014;
facilitating surveys in deeper water over larger areas (e.g. Hayes et al., this volume). Therefore, the waters respond
Hovland et al. 2002; Sumida et al. 2004; Taviani et al. 2005; faster and are more sensitive to environmental change and
Wheeler et al. 2007; Freiwald et al. 2009; Orejas et al. 2009; thus can be regarded as a miniature model ocean (Bethoux
De Mol et al. 2011; Gori et al. 2013; Savini et al. 2014; et al. 1990, 1998; Bethoux and Gentili 1996; Turley 1999).
Clippele et al. 2016; see also Angeletti et al., this volume; Lo Over the last decades, the trends of long-term warming and
Iacono et al., this volume), and in several regions, primarily saltening have been evidenced throughout the Mediterranean
due to fishing activity and fisheries research surveys where Sea (Bethoux et al. 1990; Rixen et al. 2005; Nykjaer 2009;
the bycatch of deep-sea corals has occurred (e.g. Fosså et al. Vargas-Yáñez et al. 2009). Based on model simulations, an
2002; Gass and Willison 2005; Hourigan 2009; Tracey et al. increase in sea surface temperature and sea surface salinity
2011; Clark et al. 2015). This growing knowledge of the (SST and SSS) by 2 to 3 °C and 0.48 to 0.89 are predicted for
presence and spatial distribution of CWCs allowed to model 2070–2099. This is in comparison to ~30 years of SST and
and identify the most important parameters supporting or SSS data measured between 1961–1990 (Adloff et al. 2015).
limiting CWC distribution and habitat suitability (Davies The trend has also increased at depth, where a temperature
et al. 2008; Davies and Guinotte 2011; Tracey et al. 2011; and salinity increase of 0.93–1.35 °C and 0.28 to 0.52 respec-
Rowden et al. 2013; Anderson et al. 2016). Among a multi- tively has occurred throughout the water column. At the
tude of environmental and geographic variables taken into depths that scleractinian CWCs occur in the Mediterranean
consideration depth, temperature, salinity and aragonite sat- (below 200 m), the predicted temperature rise may increase
uration state (Ωa) appear to be some of the most important by up to 2 °C and the salinity by ~0.5. Accordingly,
factors controlling the abundance and distribution of CWCs. Mediterranean CWCs might be exposed to a temperature
Additionally, the knowledge on the physiology and growth between 15.5 to 16 °C and a salinity of 39.5 to 40 by the end
of CWCs has rapidly advanced during the last decade of the century.
(Lartaud et al., this volume; Reynaud and Ferrier-Pagès, this The Mediterranean Sea is characterised by a high total
volume) owing to an increased effort in sampling live CWCs alkalinity (AT) of ca 2600 μmol kg−1 with a high buffering
and in establishing aquarium facilities that allow to maintain capacity absorbing more CO2 than the open ocean (CIESM
CWCs for an extended time in the laboratory (see Orejas 2008). It is a small to medium sink for CO2 absorbing ca.
et al., this volume and references therein). 0.24 Gt C year−1 (D’Ortenzio et al. 2008) while the reduction
520 C. Maier et al.
of ocean pH is relatively fast with −0.14 to −0.05 pH units 44.2 Ocean Acidification Studies
year−1 (Touratier and Goyet 2009, 2011). Despite this, the Ω
remains higher in the deep Mediterranean waters compared The pCO2 used in most of the OA experimental studies ranged
to the deep waters of the North Atlantic (Millero et al. 1979), between ambient (ca. 400 μatm) and 800–1000 μatm, corre-
and even at the deepest water depths the seawater is not sponding to current and future conditions in 2100 using a
likely to become undersaturated with respect to Ωa (Hassoun business-as-usual CO2 emission scenario. The exception was
et al. 2015; Goyet et al. 2016). Present day Ωa reported in the for two short-term experiments where pCO2 levels in which
vicinity of Mediterranean CWCs are relatively high ranging pCO2 values outside this range were used: 280 μatm to repre-
between 2.3 and 3.0 (Rodolfo-Metalpa et al. 2015; Maier sent pre-industrial times (Maier et al. 2012) and 1725 μatm
et al. 2016) but will drastically decrease to ca. 1.5 by the end (Maier et al. 2016). The first studies of the effect of OA were
of the century (Maier et al. 2016). performed on Lophelia pertusa. They revealed a negative
response of calcification to increasing pCO2 during short-
term exposure (Maier et al. 2009; Form and Riebesell 2012)
44.1.6 Effect of Climate Change Parameters while no effect was detected when exposed for several months
on Cold-Water Corals to elevated pCO2 (Form and Riebesell 2012). These two stud-
ies show that L. pertusa is able to maintain positive calcifica-
To date 24 experimental studies have been published on the tion rates despite being exposed to undersaturated Ωa (Maier
physiological response of scleractinian CWCs to climate et al. 2009; Form and Riebesell 2012). Subsequent studies
change and these studies, from both the Mediterranean and have demonstrated that calcification remains constant for
elsewhere, are summarised in Table 44.1. Nineteen of these pCO2 levels corresponding to those between present- day
studies addressed the effect of OA, eight the effect of tem- (~400 μatm) and those projected until the end of the century
perature, four took into account the combined effect of OA (~800–1000 μatm) (Figs. 44.1, 44.2, and 44.3). This was
and temperature. No studies are available on the effect on found for both short- and long-term exposure and for most
CWCs to changes in salinity. Interestingly, 40% of the stud- CWC species studied, suggesting that no long-term acclima-
ies were conducted using CWCs from the Mediterranean tion occurs (Maier et al. 2012, 2013b, 2016; Carreiro-Silva
Sea region. The studies comprise five scleractinian coral et al. 2014; Hennige et al. 2014; Movilla et al. 2014a, b;
species (Madrepora oculata, Lophelia pertusa, Rodolfo-Metalpa et al. 2015). However, some recent litera-
Desmophyllum dianthus, Dendrophyllia cornigera and ture states that CWCs may exhibit a long-term acclimation
Caryophyllia smithii), while most of the non-Mediterranean response in calcification to OA (Hennige et al. 2015; Roberts
CWC studies were confined to the species L. pertusa et al. 2016). Evidently, calcification is negatively affected in
(Table 44.1). The studies were distinct with respect to the short-term experiments when Ωa is below a certain threshold
time allowed for acclimation, replication and the use of sin- level (Figs. 44.1a, c and 44.2b, c; Maier et al. 2009; Lunden
gle (Fig. 44.1), consecutive (Fig. 44.2) or repeated et al. 2014; Georgian et al. 2016b, Maier et al. 2016) but the
(Fig. 44.3) measure designs. Most studies were carried out same is true in long-term experiments (Fig. 44.3d, Hennige
in the laboratory, some short-term experiments were con- et al. 2015). Furthermore, using a repeated measures experi-
ducted at sea using freshly collected specimens and seawa- mental design, Movilla et al. (2014b) showed a decline in cal-
ter from the actual sampling site (Maier et al. 2009, 2012; cification for the Mediterranean coral Desmophyllum dianthus
Hennige et al. 2014) and one other Mediterranean study after 314 days of exposure to elevated pCO2 (800 μatm),
included in situ experiments where coral fragments were while no effect at shorter exposure times was observed
transplanted to the close vicinity of a natural CO2 vent site (Fig. 44.3c; Movilla et al. 2014b). This response might be
(Rodolfo-Metalpa et al. 2015). To provide an indication on species-specific, as none of the other three species (L. per-
the statistical robustness of the experimental studies a point tusa, Madrepora oculata and Dendrophyllia cornigera) stud-
system was introduced (“SR”; Table 44.1) taking into ied in parallel revealed any significant effect between control
account criteria such as the number of replication, number and elevated pCO2 treatments, neither during short- nor long-
of repeated measurements and the type of controls. term exposure (Movilla et al. 2014a,b). It would have been
Theoretically, a minimum point score of 3 and a maximum interesting to see, if calcification of D. dianthus remains at the
of 11 was possible, and an average SR of 5.7 points lower level it revealed after 314 days, restores calcification to
(±1.4 S.D) was typical for the studies (Table 44.1). This normal rates or in the worst case scenario, further reduces
point system is not exclusive with respect to other criteria calcification with increasing exposure time. A result such as
that may be important to evaluate the robustness of a study this could be indicative of an eventual break down in calcifi-
(e.g. handling stress, sampling and analytical procedures, cation as a consequence of extended and continuous exposure
adequacy of maintenance conditions), however, these crite- to elevated pCO2. For D. dianthus it has been shown that
ria are difficult to judge in a scoring system. genes involved in stress response, metabolism or calcification
Table 44.1 Summary of experimental studies on the effects of climate change on cold-water corals (CWCs)
Reference Region Factors Species Physiol. functions Experimental design Replication
# T OA TxOA F S LP MO DE DC CS SV G R Sk GE OT † ST LT SM RM CM IC PC FC n Tanks/n SR
1 Dodds et al. (2007) N-A + − − − − + − − − − − − + − − − − + − + − − − + − 4–6 n 5
2 Maier et al. (2009) Skag − + − − − + − − − − − + − − − − − + − + − − − + − 2x8 n 6
3 Form and Riebesell N-A − + − − − + − − − − − + − − − − − + − + − − − + − 4 n 4
(2012) − + + − − − − − 5 n 4
4 Maier et al. (2012) MED − + − − − − + − − − − + + − − − − + − + − + + − − 15 n 7
5 Maier et al. (2013b) MED − + − − − + + − − − − + − − − − − + + + + − + + − 4 n 7
6 Maier et al. (2013a) MED + + + − + + − − − − − + − − − − + + + + − + + − 4 n 7
7 Brooke et al. (2013) GoM + − − − − + − − − − − − − − − − + + − + + − − + − 5 n 6
8 Naumann MED + − − − − + + − − − − + + − − DOC − − + + + − − + − 5 1/n 5
et al. (2013b)
9 Naumann MED + − − − − − − + + − − + − − − − − − + + − − − + − 5 1/n 4
et al. (2013a)
10 Carreiro-Silva et al. N-A − + − − − − − + − − − + + − + NUTS − − + + + − − + − 6 2/n 6
(2014) GE
11 Hennige et al. (2014) N-A − + − − − + − − − − − + + − − − − + − + + − + + − 8 1/n 6
12 Lunden et al. (2014) GoM + + − − − + − − − − − + − − − − + + − + − + − + − 2x8 2/n 7
13 Movilla et al. (2014a) MED − + − − − + + − − − − + − + − − − − + + + − − + − 12–18 3/n 7
14 Movilla et al. (2014b) MED − + − − − − − + + − − + − + − OM − − + + + − + + − 9 3/n 7
15 Rodolfo-Metalpa MED − + − − − − − + + + − + + − − − − − + + − − + + − 7–23 2/n 7
et al. (2015)
16 Hennige et al. (2015) N-A + + + − − + − − − − − + + + − − − − + + + − − + − 4–8 4/n 6
17 Wall et al. (2015) (#3) N-A − + − − − + − − − − − − − + − d11B − − + + − − − + − 1–4 n n/a
18 Gori et al., (2016) MED + + + − − − − + − − − + − + − − − − + + − − − + − 3 n 4
19 Maier et al. (2016) MED − + − + − − + − − − − + + − − TOC; − + − + + + + − + 13 n 9
RQ; E
20 Georgian et al. GoM − + − + − + − − − − − + + − − Food − + − + − − − + − 8 2/n 5
(2016a, b) Skag uptake
21 Büscher et al. (2017) N-A + + + + − + − − − − − + − + − RNA/ + − + + − − − + − 4 n 4
DNA
22 Kurman et al. (2017) GoM − + − − − + − − − − − + − − − GT − + − + − − − + − 12 1/n 5
+ − − − CAA + − + + + − − + − 4 1/n 4
23 Burdett et al. (2014) N-A − + − − − + − − − − − − − − − DMSP − + − + − − − + − 5 1/n 4
24 Gammon et al. (2018) SW-P − + − − − − − − − − + + + + − CS, pHi + − + + + − − + − 9 3/n 6
MED = 10 8 19 4 2 0 17 6 5 3 1 1 16 9 5 2 8 4 10 11 19 9 3 8 16 1 5.7
The variables used temperature change (T), ocean acidification (OA), combined effects of T and OA (TxOA) and salinity (S). The study regions were the Mediterranean Sea (MED), the focus region of this Chapter,
as well the North-Atlantic (N-A), Skagerrak (Skag), Gulf of Mexico (GoM) and South-West Pacific (SW-P). Study species were Lophelia pertusa (LP), Madrepora oculata (MO), Desmophyllum dianthus spp. (DE),
Dendrophyllia cornigera (DC), Caryophyllia smithii (CS) and Solenosmilia variabilis (SV). The measures of calcification (G), respiration (R), skeletal structure (Sk), gene expression (GE), genotypes (GT), polyp
mortality (†) and other measurements (OT), like inorganic nutrients (NUTS), dimethylsulfoniopropionate (DMSP), dissolved organic carbon (DOC), organic matter (OM), total organic carbon (TOC), respiratory
quotient (RQ), energy requirements (E), boron isotopes (δ11B), carbonic anhydrase activity (CAA), RNA/DNA ratio (RNA/DNA) and loss of coenosarc (CS). Experiments were evaluated according to their statistical
robustness (SR) by using a point-system based on experimental duration short- and/or long-term exposure (ST and/or LT), design with a single (SM), repeated (RM) or consecutive (CM) measurements, the type of
control(s) used with initial (IC), parallel (PC) and/or final controls (FC). The number of replicates (n), number of tanks per treatment (tanks/n) were taken into consideration. The points for statistical robustness (SR)
were attributed as follows: each “+” under Experimental Design was counted as 1. For replication 1 point was given for of 5–9 and 2 points for >10 replicates. If more than 1 tank per treatment for replicates (tanks/n)
was used (>1/n) another point was allocated
522 C. Maier et al.
5
C 5
CS 5
Fig. 44.1 Plot of studies using single-point experimental designs for Table 44.1. For studies addressing combined effects of OA and tem-
measurements according to aragonite saturation state (Ωa) in seawater perature (g) or OA, temperature and feeding (h) coloured symbols were
(y-axis) and acclimation time in days (duration of experiments [d], x used. The temperature and high or low food supply (HF and LF) are
axes). The response of physiological functions are shown according to indicated in the symbol legend. According to the region the ambient Ώa
studies (a–h) and include calcification (G), calcification of different varied and is indicated by the green area. The grey area indicates Ώa < 1.
genotypes (GGT), respiration (R), gene expression (GE), carbonic anhy- Numbers in brackets refer to the publications referenced in Table 44.1.
drase activity (CAA) and nitrate excretion (NO32−) for the species Size of symbols is indicative of number of replicates (n), vertical arrows
Lophelia pertusa (LP), Madrepora oculata (MO), Desmophyllum dian- depict where a significant positive (↑) or negative (↓) response was
thus (DE), Dendrophyllia cornigera (DC), and Caryophyllia smithii revealed, while n.s. indicates that there was no significant effect
(CS). Numbers in brackets refer to the publications referenced in between treatment levels for the respective variable (© Cornelia Maier)
were upregulated under elevated pCO2 levels after a 8-month tion of genes is dependent on the duration of exposure. While
exposure while the rates of calcification and respiration calcification rates are relatively constant over a large range of
remained stable (Carreiro-Silva et al. 2014). No time-series pCO2 and only decrease after a certain threshold has been
on gene expression experiments exist for these species to reached, faster skeletal linear extension under high pCO2 has
date, and so it is not known whether an up- or down regula- been reported for North Atlantic studies on L. pertusa
MO (4) MO-HF (19)

MO-LF (19)
Fig. 44.2 Plot of studies using consecutive experimental designs for depict the high (HF) and low (LF) food regime. According to the region
measurements according to aragonite saturation state (Ωa) in seawater the ambient Ώa varied and is indicated by the green area. The grey area
(y-axis) and acclimation time in days (duration of experiments [d]; x indicates Ώa < 1. Numbers in brackets refer to the publications refer-
axes). The symbol lines record changes of Ωa during experiments with enced in Table 44.1. Size of symbols is indicative of number of repli-
symbols depicting when calcification (G) or respiration (R) of Lophelia cates (n), vertical arrows depict where a significant positive (↑) or
pertusa (LP) or Madrepora oculata (MO) were assessed during the negative (↓) response was revealed, while n.s. indicates that there was
consecutive changes in Ωa. Numbers in brackets refer to the publica- no significant effect between treatment levels or time steps for the
tions referenced in Table 44.1. Coloured symbols (in h) were used to respective variable (© Cornelia Maier)
LP (11) LP (5, 6) LP 9°C (16)

MO (5, 6) DC (13) MO (14) LP 12°C (16)
DE (13) LP (14)
Fig. 44.3 Plot of studies using repeated measurement designs and is indicated by the green area. The grey area indicates Ώa < 1.
showing measurements points according to aragonite saturation Numbers in brackets refer to the publications referenced in
state (Ωa) in seawater (y-axis) and acclimation time in days (dura- Table 44.1. Coloured symbols were used for the combined effect of
tion of experiments [d]; x-axis). The symbol lines record Ωa for rep- OA and temperature (in d) with the temperature indicated in the
licated measurements with symbols depicting when calcification (G) symbol legend. Size of symbols is indicative of number of replicates
or respiration (R) of L. pertusa (LP), M. oculata (MO), D. dianthus (n), vertical arrows depict where a significant positive (↑) or nega-
(DE) or D. cornigera (DC) were assessed during the consecutive tive (↓) response was revealed, while n.s. indicates that there was no
changes in Ωa. Numbers in brackets refer to the publications refer- significant effect between treatment levels or time steps for the
enced in Table 44.1. According to the region the ambient Ώa varied respective variable (© Cornelia Maier)
524 C. Maier et al.
(Hennige et al. 2015). This coincides with thinner and longer might occur in favor of other physiological functions that may
corallites and an altered mineral organisation that may impact explain the observed decline in calcification of D. dianthus
the stability and breaking strength of the skeleton and the sta- (Movilla et al. 2014b). The decrease in skeletal colouration
bility of the CWC framework. Despite this, changes in the attributed to a loss of coenochyme seen by Gammon et al.
micro-density and porosity were not reported under similar (2018) may have also reflected a food scarcity response.
conditions, neither for North Atlantic L. pertusa (Wall et al.
2015) nor Mediterranean CWC species (Movilla et al. 2014a).
In a study on a related species Solenosmilia variabilis colo- 44.2.1 Temperature
nies were grown under ambient pH (7.88, Ωa 0.93) and lower
pH (7.65, Ωa 0.78) for two years (Gammon et al. 2018). Of the eight studies assessing the response of CWCs to
Respiration and growth rate were not altered under low pH, changes in temperature, two measured the survival of L. per-
although there was a decrease in skeletal colouration attrib- tusa from the Gulf of Mexico at a temperature range from 8
uted to a loss of coenochyme, the tissue connecting neigh- (ambient) to 15, 20 and 25 °C and an exposure time of 1 and
bouring polyps and covering the outer skeleton, indicating the 8 days (Brooke et al. 2013) or by changing temperature in
potential reallocation of energy to other physiological pro- consecutive steps from 8, 10, 12, 14 to 16°, with an adjust-
cesses such as growth and respiration. While there has been ment period of 1 day per 2 °C increment (Lunden et al.
two studies where respiration decreased or increased after 2014). Both studies showed significant mortalities at tem-
two weeks during short-term exposure to higher pCO2 peratures ≥15 °C and conclude that the upper temperature
(Figs. 44.1c and 44.3a; Hennige et al. 2014; Georgian et al. limit for the survival of L. pertusa would be 15 °C. The pro-
2016b) no effect on respiration at increased pCO2 levels has jected rise in temperature in the Mediterranean Sea could be
been detected in other studies (Figs. 44.1e–g, 44.2c, and as detrimental to the Mediterranean CWCs. However, the
44.3b, c; Maier et al. 2013a, 2016; Carreiro-Silva et al. 2014; experimental design used by Brooke et al. (2013) did not
Movilla et al. 2014a, b; Rodolfo-Metalpa et al. 2015; Hennige allow for longer term acclimation and was in fact designed to
et al. 2015; Gori et al. 2016; Gammon et al. 2018). reflect specific conditions prevailing in the Gulf of Mexico,
The apparent high resilience of CWCs to OA in both the where CWCs can experience occasional flushing by warm-
experimental studies, described here for the Mediterranean water currents and a rapid and dramatic increase in seawater
and elsewhere, and also observed in situ (Thresher et al. 2011; temperature (Brooke et al. 2013). In the Mediterranean Sea,
Fillinger and Richter 2013; Jantzen et al. 2013; Bostock et al. CWCs are not subject to such an abrupt temperature increase,
2015; Georgian et al. 2016a; Gammon et al. 2018) has been but they are subject to the high temperatures at the extreme
attributed to pH upregulation of the calicoblastic pH reported for all CWCs. It is for this reason that it has been
(McCulloch et al. 2012; Wall et al. 2015). The upregulation of assumed that the Mediterranean CWCs are already at their
calicoblastic pH has been thought to require a high amount of upper tolerance limit (ca. 13 °C) and any further increase in
energy and may consequently require high food availability in temperature might therefore be detrimental. Despite this,
areas with low Ωa to maintain calcification constant there is some evidence that Mediterranean CWCs are well
(McCulloch et al. 2012; Fillinger and Richter 2013; Jantzen adapted to a relatively constant high temperature. In two
et al. 2013). However, a study establishing an energy budget experiments without prior acclimation phase, a temperature
for major physiological functions of Mediterranean M. ocu- dependent increase or decrease of respiration has been
lata revealed that the energy required for calcification in gen- reported for L. pertusa from the North Atlantic (Dodds et al.
eral and for the upregulation of calicoblastic pH (or Ωa) in 2007) and Mediterranean Sea (Maier et al. 2013a, Supplement
particular only constitutes a minor fraction of about 1 to 3% of SI_1). At ambient temperature, respiration rates of
overall metabolic requirements (Maier et al. 2016). Despite a Mediterranean L. pertusa were comparable to those from the
four-fold food uptake in the high feeding group and the respi- North Atlantic region despite the 4 °C temperature differ-
ratory quotient indicating starvation in the low-food group, no ence. The temperature-dependent coefficient of respiration
mitigating effect on calcification or respiration at increased (Q10) was lower for Mediterranean L. pertusa than for North-
pCO2 levels due to feeding was reported (Maier et al. 2016). Atlantic specimen further indicating that Mediterranean L.
Similarly, in a study on North-Atlantic L. pertusa no mitigat- pertusa as being well adapted to the higher temperature and
ing effect of feeding has been shown despite a tenfold food potentially less sensitive to a further increase in temperature
availability in the high-food group (Büscher et al. 2017). than specimen from colder regions. This is further substanti-
However, the need to double the energy allocated to calcifi- ated by the finding by Naumann et al. (2013a, b) and Hennige
cation at elevated pCO2 (Maier et al. 2016) might nevertheless et al. (2015) who found that no significant changes in respi-
constitute a burden over an extended time and permanent expo- ration were observed when Mediterranean or North Atlantic
sure to unfavorable conditions. Specifically in an environment L. pertusa were acclimated for 3–6 months to lower or higher
where food is permanently scarce, a shift in energy allocation than ambient temperatures (Naumann et al. 2013a, b;
Hennige et al. 2015). However, in the study by Hennige et al. pCO2 levels representative of projected changes in the
(2015) respiration rates decreased significantly after a total Mediterranean Sea. However, the statistical robustness of the
of 9 months exposure to 12 °C. This response is difficult to experiment was limited, due to a low number of sample rep-
explain, and with the good replication (n = 8, 4 tanks / n) it is licates (n = 3) (Table 44.1). The results are useful as they
not likely caused by experimental constraints such as tank provide a first indication as to how Mediterranean D. dian-
effects. The authors therefore consider “… that normal’ thus would respond to long-term increasing temperature;
energetic strategies are no longer applying, possibly due to however the results require some consolidation.
other processes using energetic reserves. This could be the This can also be said for the general perception that
result of processes that maybe occurring of which we have CWCs in the Mediterranean Sea are at their upper tolerance
poor understanding and/or cannot easily measure” (Hennige limit with respect to temperature. There is evidence that at
et al. 2015). In contrast to L. pertusa, respiration of least some of the species may be able to cope with increasing
Mediterranean M. oculata significantly decreased when tem- temperatures but overall there needs to be some caution
perature was lowered from 12 to 9 and then down to 6 °C before drawing this conclusion. It is important to consider in
after a 3-month acclimation (Naumann et al. 2013b). This the first instance experimental design (duration of experi-
result led the authors to speculate that M. oculata acclimates ments, sample sizes, replication, and controls), as well as
at a much slower rate to changes in temperature than L. per- other environmental stressors, before any assumptions can
tusa. The results also provide the variable thermal tolerance be made when assessing the physiological response of these
range for the two species. M. oculata is the dominant species corals to changes in temperature.
in the Mediterranean, while L. pertusa prevails in colder
regions like the North Atlantic. This preferred distribution
for both species could indicate that L. pertusa acclimates 44.2.2 Salinity
faster to colder temperature than M. oculata and conversely,
that M. oculata acclimates more easily to increasing tem- As a consequence of global change, the salinity in the
peratures. To date, no longer term study with respect to Mediterranean Sea will increase by ~0.5 at the depths of
increasing temperature tolerance exists for these two species CWC occurrence (see Skliris, this volume and references
and no final conclusion can be made as to: how these two herein). Despite this fact, and that the current salinity levels
species may acclimate to the ongoing warming in the are the highest reported for CWC occurrence in any one area,
Mediterranean Sea. For calcification responses, the no studies are available on the physiological response of
Mediterranean D. cornigera revealed a significant increase CWCs to increasing salinity. In addition to this and of sig-
in calcification at 17.5 °C while a slight but non-significant nificance is that climate change models need to take into
reduction to 83% was reported for D. dianthus at 17.5 °C account the ever growing need of freshwater in this region as
(Naumann et al. 2013a). When the temperature was lowered consequence of a growing population and a higher consump-
from 12 to 9 to 6 °C, calcification of M. oculata and L. per- tion per capita. The construction of desalination plants along
tusa was faster at the higher temperature levels in both spe- Mediterranean shorelines has intensified during the last
cies. While calcification of M. oculata significantly decreased decades several times over to generate fresh water. While
at each temperature step, calcification of L. pertusa was only 50% of the seawater is converted to drinking water the other
significantly lower at 6°, and between 12 to 9 °C only a 50% is discharged back into the sea as concentrated brine.
slight, non-significant decrease was observed (Naumann For the Mediterranean Sea, it has been estimated that the
et al. 2013b). For North Atlantic L. pertusa the response salinity due to brine discharge will increase by an additional
differed, showing a slight decrease in calcification to 82 and 0.81 g / L until 2050 (Bashitialshaaer et al. 2011). This situ-
70% after exposure of 3 and 6 months to higher (12 °C) than ation means that together with the salinity increase due to
ambient (9 °C) temperature, while calcification increased to climate change, the salinity may rise to above levels of
1.5 times that at ambient temperature after a total of 9 months around 40, which is comparable to the salinity of the Red
(Hennige et al. 2015, Fig. 44.3d). The study on Mediterranean Sea. The Red Sea is renowned for its thriving tropical coral
D. dianthus by Gori et al. (2016) reported a significant and reefs and one may therefore speculate that this increase in
negative effect on calcification when temperature was salinity may not impact Mediterranean CWCs. However, a
increased from 12 to 15 °C. When subjected to both elevated high sensitivity to small changes in salinity has been reported
temperature and pCO2, however, there was no significant cal- for the tropical coral S. pistillata found in the region and that
cification effect and the opposite result was found for respi- appeared to acclimate more easily to a decline than to an
ration (Gori et al. 2016). The experimental approach of the increase in salinity (Ferrier-Pagès et al. 1999). As with tem-
Gori et al. (2016) study was interesting and timely as the perature, salinity is the highest reported in the Mediterranean
authors tackled the question of single and combined effects region experienced by CWC habitats to date. It will therefore
of temperature and OA impacts with the temperature and be important to study the response of Mediterranean CWCs
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Drop Chapter
A Case Study: Variability 45
in the Calcification Response
of Mediterranean Cold-Water Corals
to Ocean Acidification
Juancho Movilla
Abstract the Mediterranean than in the global ocean (Touratier et al.

The Mediterranean Sea has certain characteristics that 2012; Palmiéri et al. 2015), it is expected that this threat will
make it especially sensitive and vulnerable to changes in be an added pressure to other anthropogenic influences and
atmospheric CO2 and its gradual acidification. Some of extreme natural events taking place at present in this semi-
the organisms that may be the first to be threatened by this enclosed sea (Calvo et al. 2011).
impact are the cold-water corals. The few studies carried Given the lack of fundamental information on the biologi-
out up to date with these organisms by simulating in cal impacts of OA on CWC communities, experimental
aquarium the acidified conditions expected for the year manipulations in aquaria will continue to play an important
2100 revealed a high variability between and within spe- role in improving our knowledge on this topic (Orejas et al.,
cies. This chapter shows this highly variable response in this volume). However, due to the difficulties of sampling in
the calcification of four of the most abundant cold-water deep-sea areas, only a handful of studies have focused on eval-
coral species in the Mediterranean to low-pH conditions uating such effects in Mediterranean CWC, with rather differ-
and their potential ecological implications. ent results (Maier et al. 2012, 2013; Rodolfo-Metalpa et al.
2015; see Maier et al., this volume for a review). In the follow-
Keywords ing, laboratory experimentation is used to illustrate the high
Ocean acidification · Mediterranean · Lophelia pertusa · variability between and within Mediterranean CWC species
Madrepora oculata · Dendrophyllia cornigera · with regard to calcification responses to low-pH conditions.
Desmophyllum dianthus We conducted experiments simulating the present pH val-
ues and those expected by the year 2100 to assess the response
to OA of four of the most widely distributed CWC species in
In the upper bathyal zone of the Mediterranean Sea (between the Mediterranean (L. pertusa, M. oculata, D. cornigera and
~200 and 1200 m depth), Lophelia pertusa, Madrepora ocu- D. dianthus; Fig. 45.1). For further details on the experimen-
lata, Dendrophyllia cornigera and Desmophyllum dianthus tal setup, see Movilla et al. (2014a, b). Interestingly, no appar-
are the principal cold-water coral (CWC) species, which ent pH-driven effects on the calcification process were
form three-dimensional structures (especially Lophelia and observed in L. pertusa and M. oculata at midterm (6 months)
Madrepora) that host an enormous variety of associated spe- and D. cornigera at long-term (11 months) exposure time,
cies (Orejas et al. 2009; Gori et al. 2013; Roberts and Cairns compared to control conditions (Fig. 45.2). However, we
2014; D’Onghia et al., this volume; Rueda et al., this vol- found a high intraspecific variability in the calcification rate
ume). Regrettably, ocean acidification (OA) could lead to among different colony fragments of L. pertusa depending on
degradation and fragmentation of these deep-sea habitats their initial weight, with small and younger nubbins showing
(Roberts et al. 2006; Cao et al. 2014). Moreover, although it faster skeletal growth rates. It is expected that those younger
is still under debate if the impact of OA will be stronger in specimens with high calcification rates may be the most sus-
ceptible to the negative effects of OA due to the high-energy
demand of this biological process (Cohen and Holcomb 2009;
J. Movilla (*) Allemand et al. 2011). This hypothesis was supported by the
Instituto Español de Oceanografía, Centro Oceanográfico de response observed in D. dianthus to low-pH conditions pre-
Baleares, Estación de Investigación Jaume Ferrer, Menorca, Spain
dicted for 2100. Fast-growing young polyps of D. dianthus
Instituto de Ciencias del Mar (ICM-CSIC), Barcelona, Spain displayed a 70% reduction in their calcification rates after a

https://doi.org/10.1007/978-3-319-91608-8_45
532 J. Movilla
Fig. 45.1 Specimens of

Lophelia pertusa (a),
Madrepora oculata (b),
Desmophyllum dianthus (c,
left) and Dendrophyllia
cornigera (c, right) in the
experimental aquaria. Photo
credits by A. Gori (a and b)
and E. Obis (c). Panel (a)
previously published by
MEPS (©Inter-Research
2011)
Fig. 45.2 Calcification rates

under control (pH
~8.10 units) and acidified
conditions (pH ~7.81 units).
Results are expressed as
mean ± SE. Asterisk indicates
significant differences
between treatments
45 Calcification Response of Cold-Water Corals to Ocean Acidification 533
long-term (11 months) exposure to acidified conditions, Calvo E, Simó R, Coma R, et al (2011) Effects of climate change on
Mediterranean marine ecosystems: the case of the Catalan Sea.
whereas larger and older polyps showed no significant effects Clim Res 50:1–29
to pH reduction. Cao L, Zhang H, Zheng M, et al (2014) Response of ocean acidification
These results suggest some degree of acclimation in terms to a gradual increase and decrease of atmospheric CO2. Environ Res
of calcification to changes in carbonate chemistry and no Lett 9:024012
Carreiro-Silva M, Cerqueira T, Godinho A, et al (2014) Molecular
mid- to long-term effects of OA in CWC populations when mechanisms underlying the physiological responses of the cold-
assessing the average overall effect on large adult colonies. water coral Desmophyllum dianthus to ocean acidification. Coral
However, those CWC populations presenting younger coral Reefs 33:465–476
colonies with small polyps may be more sensitive to Cohen AL, Holcomb M (2009) Why corals care about ocean acidifica-
tion: uncovering the mechanism. Oceanography 22:118–127
OA. These young, fast-growing polyps ensure, in the case of Gori A, Orejas C, Madurell T, et al (2013) Bathymetrical distribution
the branching CWC colonies, the increase in size and com- and size structure of cold-water coral populations in the Cap de
plexity of the three-dimensional structures. Similarly, in the Creus and Lacaze-Duthiers canyons (northwestern Mediterranean).
case of the solitary corals such as D. dianthus, the young Biogeosciences 10:2049–2060
Hennige SJ, Wicks LC, Kamenos NA, et al (2015) Hidden impacts of
polyps are the recruits, which support the maintenance of the ocean acidification to live and dead coral framework. Proc R Soc B
populations. Thus, the decreased in calcification of these 282:20150990
young polyps could compromise the long-term persistence Maier C, Watremez P, Taviani M, et al (2012) Calcification rates and
of CWC communities and the habitats they form in the the effect of ocean acidification on Mediterranean cold-water corals.
Proc R Roc B 279:1716–1723
Mediterranean. Maier C, Schubert A, Berzunza-Sánchez MM, et al (2013) End of the
We should keep in mind that although calcification rates century pCO2 levels do not impact calcification in Mediterranean
did not change between treatments, other adverse effects cold-water corals. PLoS One 8:e62655. https://doi.org/10.1371/
associated with a lower pH could also be at stake. Indeed, it journal.pone.0062655
Movilla J, Gori A, Calvo E, et al (2014a) Resistance of two Mediterranean
is known that OA could affect CWC in different ways (e.g. cold-water coral species to low-pH conditions. Water 6:59–67
Carreiro-Silva et al. 2014; Hennige et al. 2015; Maier et al., Movilla J, Orejas C, Calvo E, et al (2014b) Differential response of two
this volume) and that synergies with other stressors could Mediterranean cold-water coral species to ocean acidification. Coral
make them more susceptible to other threats (e.g. Wicks Reefs 33:675–686
Orejas C, Gori A, Lo Iacono C, et al (2009) Cold-water corals in the Cap
and Roberts 2012). On the other hand, even in the case de Creus canyon, northwestern Mediterranean: spatial distribution,
where a given species shows a strong and consistent density and anthropogenic impact. Mar Ecol Progr Ser 397:37–51
response to acidification, reactions may be significantly Palmiéri J, Orr JC, Dutay JC, et al (2015) Simulated anthropogenic CO2
different at the community level. This ‘scaling up’ from storage and acidification of the Mediterranean Sea. Biogeosciences
12:781–802
individual to community or ecosystem level is one of the Roberts JM, Cairns SD (2014) Cold-water corals in a changing ocean.
most challenging goals in assessing the effects of OA. It is Curr Opin Environ Sustain 7:118–126
important to evaluate jointly the physiological response of Roberts JM, Wheeler AJ, Freiwald A (2006) Reefs of the deep: the
several key species under future conditions, as well as iden- biology and geology of cold-water coral ecosystems. Science
312:543–547
tify the eventual consequences related with changes on spe- Rodolfo-Metalpa R, Montagna P, Aliani S, et al (2015) Calcification is
cies interaction and energetic flow thorough trophic webs. not the Achilles’ heel of cold-water corals in an acidifying ocean.
An integrative understanding how the ecosystem works as Glob Chang Biol 21:2238–2248
a whole is essential to predict the consequences of the dif- Touratier F, Guglielmi V, Goyet C, et al (2012) Distributions of the car-
bonate system properties, anthropogenic CO2 and acidification dur-
ferent stressors that are affecting the marine biodiversity of
ing the 2008 BOUM cruise (Mediterranean Sea). Biogeosci Discuss
the Mediterranean Sea. 9:2709–2753
Wicks L, Roberts JM (2012) Benthic invertebrates in a high-CO2
Acknowledgements I wish to thank E. Calvo and C. Pelejero for their world. Oceanogr Mar Biol Annu Rev 50:127–188
supervision throughout the experimental phase. Constructive comments
by M. Carreiro-Silva and S. Hennige greatly improved this chapter.
This research was supported by the European Projects HERMES
(Goce-CT-2005-511234-I), HERMIONE (Grant Agreement Number Cross References
226354), the Spanish Projects CTM2009-08849/MAR and
CTM2012- 32017 and by the Marine Biogeochemistry and Global D’Onghia G (this volume) Cold-water coral as shelter, feeding and life-
Change research group (Generalitat de Catalunya, 2009SGR142). history critical habitats for fish species: ecological interactions and
fishing impact
Maier C, Weinbauer MG, Gattuso JP (this volume) Fate of Mediterranean
scleractinian cold-water corals as a result of global climate change.
References A synthesis
Orejas C, Taviani M, Ambroso S, et al (this volume) Cold-water coral
in aquaria: advances and challenges. A focus on the Mediterranean
Allemand D, Tambutté E, Zoccola D, et al (2011) Coral calcification,
cells to reefs. In: Dubinsky Z, Stambler N (eds) Springer, Dordrecht,
pp 119–150. https://doi.org/10.1007/978-94-007-0114-4
Conservation of Cold-Water Corals
in the Mediterranean: Current Status 46
and Future Prospects for Improvement
Maria del Mar Otero and Pilar Marin
Abstract Keywords
The Mediterranean deep-sea contains a mosaic of ecosys- Cold-water corals · Mediterranean · Marine conservation
tems and habitat types. Among them, cold-water corals · Policy · Species protection · Deep-sea
provide shelter to a large and unique variety of organisms
as well as ecosystem services. Scientific findings over the
last decade have strengthened this fact and further sup-
ported the identification of cold-water corals habitats as 46.1 Introduction
sites of conservation interest and high vulnerability. Given
the semi-enclosed nature of the Mediterranean basin and Knowledge of global cold-water coral (CWC) ecosystems
the significant anthropogenic pressure on its ecosystems, has significantly increased over the last two decades. New
most, cold-water corals species have been listed as threat- findings have increased our information on the occurrence
ened as they are found at areas which are frequently the and spatial distribution of deep-sea corals (see Altuna and
focus of resource exploitation (e.g. deep-sea fisheries, oil Poliseno, this volume, and references therein; Chimienti
and gas prospections among others) or are affected directly et al., this volume, and references therein), leading to a better
by other human activities (e.g. marine debris, pollution understanding of their ecological role and functional signifi-
events) as well as by the increasing impacts of climate cance. Even so, public awareness is still a pending issue (see
change including ocean acidification. Nowadays, conserva- Rossi and Orejas, this volume).
tion and protection of such important species and ecosys- Generally, CWCs refers to azooxanthellate species of
tems largely depend upon the proper development and scleractinian, antipatharian, gorgonian and stylasterid corals
implementation of marine policies. Here, we analyze the that are not restricted to the photic zone (Roberts et al. 2009),
most important policy framework in place to protect these usually found below 200 m. However, there is not a single
species in the Mediterranean Sea and we consider the most definition for the term “Cold-water corals” and several
recent developments and opportunities for improving the authors come out with different definitions, depth and tem-
situation. The management of cold-water corals involves perature limits (see for instance Cairns 2007; Altuna and
important challenges. This is partly due to their remote Poliseno, this volume, among others). CWCs have been
location, limited political awareness, as well as incomplete described in the Mediterranean Sea forming a large variety
information available on the occurrence, distribution and of biotopes with biodiversity and abundance of the dominant
resilience of these cold-water coral species and their asso- and associated species varying with the region, hydrody-
ciated fauna, to impacts and disturbances. Specific actions namic regime, topography, substrate and bathymetry among
are discussed to increase the protection of deep-sea ecosys- others (e.g. Freiwald et al. 2009; Taviani et al. 2011, 2017;
tems hosting cold-water corals through good governance Sanfilippo et al. 2013; Gori et al. 2013; Altuna and Poliseno,
and to establish effective area-based conservation measures this volume; Chimienti et al., this volume; Rueda et al., this
to safeguard Mediterranean deep-sea biodiversity. volume). Mediterranean CWCs are known to occur at the
shelf breaks, escarpments and submarine canyon walls, sea-
M. del M. Otero (*) mounts as well as on top and flanks of coral-formed reliefs or
IUCN Center for Mediterranean Cooperation, Malaga, Spain mounds. Whether they are scleractinian frameworks, dense
aggregations of antipatharians and/or gorgonians on hard or
P. Marin soft substrates, CWCs could form oasis-like habitats in the
Oceana, Europe, Madrid, Spain

https://doi.org/10.1007/978-3-319-91608-8_46
536 M. del M. Otero and P. Marin
deep Mediterranean environment providing a physical sup- face sediments, generating increased turbidity also far from
port, refuge or nursery area for other living organisms fishing grounds (Puig et al. 2012; Martín et al. 2014; Paradis
(Maynou and Cartes 2011; Baillon et al. 2012; Calcinai et al. et al. 2017). The settling of this suspended sediment (added
2013; Bo and Bavestrello, this volume; Gori et al., this vol- to the natural deposition of sediments) can lead to the smoth-
ume; Rueda et al., this volume). ering of benthic communities as have been already observed
The discovery of new CWC taxa is still ongoing as explo- at various sites such as La Fonera Canyon on the Catalan
ration of the deep Mediterranean waters continues. New spe- margin off the NW Mediterranean (Paradis et al. 2017).
cies have been discovered in recent surveys such as the soft Accidental bycatch of black corals and scleractinians with
corals Chironephthya mediterranea and Nidalia studeri experimental long lines and through trammel nets has also
reported in the shelf break and flanks of a submarine canyon been proved to have a significant impact (D’Onghia et al.
of Menorca Channel, Balearic Islands (López-González 2010, 2012; Mytilineou et al. 2014; Bo et al. 2014; Bo and
et al. 2015; see also Altuna and Poliseno, this volume). Bavestrello, this volume; Gori et al., this volume; Orejas
Often, explorations indicate also that some deep coral spe- et al., this volume). Lost fishing gears can further entangle on
cies appear to be much more extensively distributed than pre- scleractinian CWCs and damage colonies which may in turn
viously thought. This is the case of the gorgonian severely impair their recovery (Reed et al. 2007; Orejas et al.
Dendrobrachia bonsai reported in various locations along 2009; Huvenne et al. 2016).
the western coast of Corsica Island between 200 and 500 m Other aspects that are having or will have a high impact in
depth that establish its northern distribution limits in the Mediterranean CWC communities are climate change and
western Mediterranean basin (Sartoretto 2012; Altuna and ocean acidification (OA) (e.g. Maier et al. 2012; Movilla
Poliseno, this volume). Similarly, recent findings of et al. 2014a, b; Maier et al., this volume; Movilla, this vol-
Dendrophyllia ramea in Cyprus (Orejas et al. 2017, this volume), as well as the accumulation of marine litter (Savini
ume; Altuna and Poliseno, this volume) and Lebanese waters et al. 2014; Lastras et al. 2016) and chemical pollution (e.g.
(Aguilar pers. comm.1) demonstrate a new depth and geo- disposal of solid waste from land-based mines and oil spills)
graphical limit for this species. (Larsson and Purser 2011; Fabri et al. 2014; Otero et al.
Moreover, molecular identification tools are revealing a 2016).
much more diverse and evolutionarily complex picture of the Climate change is affecting the Mediterranean biodiver-
Mediterranean coral diversity than previously depicted sity (e.g. Danovaro et al. 2004; Lejeusne et al. 2010; Crisci
(Boavida et al., this volume). Debate on taxonomic re- et al. 2011; Otero et al. 2013; Parravicini et al. 2015) and it is
arrangement of some taxa, discovery of new species, as well expected to have a strong effect in the future (Giorgi 2006;
as the possibility of splitting taxa into different groups (such IPCC 2007, 2013). Current climate model simulations indi-
as in the case of the bamboo coral Acanella arbuscula from cate a significant warming, increasing acidification and tem-
Isidella elongata), are still ongoing (Heestand Saucier 2016; perature stratification, variations in precipitation patterns and
Otero et al. 2016). These studies will have a considerable terrestrial nutrient loads, as well as changes in plankton phe-
impact on conservation and management efforts and raise nology and spatial distribution among others (Yang and
the need for a more pro-active approach to safeguard the Rudolf 2010; Lazzari et al. 2014; Lacoue-Labarthe et al.
Mediterranean deep-sea biodiversity. 2016). These changes may shift the carbon balance in the sea
and further affect corals’ ability to grow as well as enhance
their vulnerability to OA (Davies et al. 2017). Ocean acidifi-
46.2 Current Impacts and Scenario Trends cation causes the depth of carbonate compensation (the spe-
cific depth at which calcium carbonate minerals dissolve in
Past and ongoing human activities impacting the the water) to rise closer to the sea surface. Consequently this
Mediterranean deep-sea have been increasingly documented will affect the rate of supply of calcium carbonate needed for
and future trends in most maritime sectors indicate that these the coral’s skeletal structures (Harris and Whiteway 2011).
impacts are on the rise (Pianté and Ody 2015). Mediterranean Cold-water corals seem to live close to their upper ther-
CWCs face considerable threat from fishing activities par- mal limits in the Mediterranean Sea (see Maier et al., this
ticularly from demersal fisheries (Maynou and Cartes 2011). volume) and are characterised by slow growth rates and long
Bottom contact gears directly damage corals (Palanques generation times (Orejas et al. 2008, 2011a, b; Lartaud et al.
et al. 2006; D’Onghia et al. 2016; Bo and Bavestrello, this 2013, 2014, 2017, this volume; Reynaud and Ferrier-Pagès,
volume; Puig and Gili, this volume) and remobilise soft sur- this volume). The detrimental effects of a potential addi-
tional stresses given by a small increase of water temperature,
lowered pH and reduced food supply are likely to reduce
Deep Sea Lebanon Project, a partnership between Oceana, IUCN and
1
UNEP/MAP-RAC/SPA, on behalf of the Ministry of Environment with their resilience and recovery capacity from other impacts
the support of CNRS-L. (e.g. Gori et al. 2016). Knowledge of the severity of these
46 Conservation of Cold-Water Corals in the Mediterranean 537
threats is further hampered by the limited knowledge of the preserve at least 10% of coastal and marine areas by 2020
occurrence, distribution and habitat requirements of CWCs (Rees et al. 2018), through especially areas of particular
(Tittensor et al. 2010). importance for biodiversity and ecosystem services, giving
Off-shore oil exploration and exploitation activities are particular emphasis to protect critical ecosystems such as
also booming in the Mediterranean basin and could increase CWC reefs and seamounts (CBD COP11 Decision XI/16).
by 60% by 2020 as gas production could increase five-folds However, the mid-term assessment of progress towards the
by 2030 (Pianté and Ody 2015). The scarce scientific infor- implementation of Aichi Targets (Global Biodiversity
mation (see Larsson and Purser 2011 work on the NE Atlantic Outlook 4) concluded that regarding Target 11 “Marine pro-
and De Leo et al. 2016 in the Gulf of Mexico) on the ecologi- tected areas are accelerating but extrapolations suggest we
cal consequences and the risks involved in developing some are not on track to meet the target. With existing commit-
of these activities would likely not be countenanced in a ter- ments, the target would be met for territorial waters but not
restrial environment and there are still significant gaps in our for exclusive economic zones or high seas” (Secretariat of
knowledge of anthropogenic impacts on the deep-sea. the Convention on Biological Diversity 2014). Likewise, the
Proposals for the commercial mining of deep-sea mineral current priority actions to achieve Aichi Target 10 for “coral
resources (particularly for sulphide deposits) in the reefs and closely associated ecosystems” are consistent with
Mediterranean Sea are not yet developed and there is great the previous work plan to avoid the physical degradation and
uncertainty concerning these exploitations. Even if the sea- destruction of coral reefs, including CWCs (appendix 1 and
floor mining is not directly developed in the vicinity of CWC 2 of annex I to decision VII/5). Moreover, this work plan
communities, it could impact suspension-feeding corals liv- aims to minimise the multiple anthropogenic pressures on
ing on rocky seafloors far from the exploitation areas, as coral reefs and other fragile ecosystems impacted by climate
already demonstrated by Larsson and Purser (2011) in the change, including OA.
NE Atlantic and by Reichelt-Bruschett (2012) in Indonesia. Furthermore, within the CBD context, it must be under-
lined that the Ecologically and Biologically Significant
Marine Areas (EBSA) process in the Mediterranean was
46.3 P
olicy Framework in Cold-Water Coral triggered by a regional workshop in 2014 (CBD 2014). The
Conservation and Management process culminated at the CBD 12th COP with the endorse-
ment of 15 EBSAs which include a wide coverage of off-
To date, Sustainable Development Goals (SDGs) have been shore areas, recognising the biological and ecological
defined as the environmental reference for United Nations significance of deep-sea habitats in the Mediterranean basin
(UN) during the period 2015–2030. Regarding marine issues, to define future manage measures that ensure the biodiver-
the global framework to develop policies and actions is pro- sity conservation of these areas.
vided by SDG 14 to “conserve and sustainably use the Today, the implementation of such international policies
oceans, seas and marine resources for sustainable develop- and targets through real management measures in the
ment (Rees et al. 2018)”. Accordingly, SDG 14 has been Mediterranean Sea is still limited. Regional and international
recently integrated in the different Mediterranean regional bodies have developed instruments and tools towards the
seas strategies for their future plans (GFCM Mid-Term achievement of these targets (Table 46.1). Analysis of those
Strategy 2017–2020; UNEP-MAP Mediterranean Strategy efforts and achievements provide the identification of further
for Sustainable Development 2016–2025). ways needed to move forward.
The United Nations General Assembly (UNGA) in para- At a regional level, within the framework of the Barcelona
graph 51 of its resolution 58/240 (2003), “reiterated its call Convention (Convention for the Protection of the Marine
for urgent consideration of ways to integrate and improve, on Environment and the Coastal Region of the Mediterranean),
a scientific basis, the management of risks to the marine bio- it is the Protocol concerning Specially Protected Areas and
diversity of seamounts, CWC reefs and other underwater Biological Diversity (SPA / BD Protocol) adopted in 1995,
features”. This further relates to the conservation and sus- which establishes the framework for the protection and con-
tainable use of biodiversity in marine areas beyond the limits servation of biodiversity of valuable areas and species in the
of national jurisdiction (ABNJ), in particular since negotia- Mediterranean Sea. This Protocol also serves as main tool
tions to develop a new instrument that addresses marine pro- for implementing the CBD with regards the sustainable man-
tected areas (MPAs) and environmental impact assessments agement of coastal and marine biodiversity. Since its adop-
in these areas, are still ongoing (Druel and Gjerde 2014; tion, several amendments have been adopted by Contracting
Blasiak and Yagi 2016). Parties, bringing the number of species listed as endangered
In addition, within the Convention on Biological Diversity or threatened in Annex II (algae, sponges, fish, mollusks,
(CBD) and its Strategic Plan for Biodiversity 2011–2020, the birds, marine mammals…) up to more than 150, and the
Aichi Target 11 called on Contracting Parties to commit to number of species listed in Annex III, referring to exploited
Table 46.1 Current policies and framework that includes protection of Table 46.2 Deep-sea anthozoan species listed as ‘Threatened’ at
CWCs in the Mediterranean Sea Mediterranean regional level (IUCN Red List, 2016) and included in
Legal or reference Species protected / Habitat that are or Annexes of the Protocol SPA/BD to Barcelona Convention (2017)
instrument can be considered Species name IUCN Red List category Protocol SPA/BD
FAO/global Isidella elongata CR Annex IIa
International guidelines Certain CWCs – communities and Corallium rubrum EN Annex III
for the Management of habitat forming species that are Leiopathes glaberrima EN Annex II
Deep-sea Fisheries in the documented or considered sensitive Desmophyllum dianthus EN Annex IIa
high seas and potentially vulnerable to deep-sea
Lophelia pertusa EN Annex II
fisheries in the high-seas, and which
may contribute to forming VMEs: Dendrophyllia cornigera EN Annex IIa
stony corals (Scleractinia) Madrepora oculata EN Annex II
alcyonaceans and gorgonians Funiculina VU
(Octocorallia) quadrangularis
black corals (Antipatharia) Pennatula phosphorea VU
Barcelona Convention/Mediterranean region Pteroeides spinosum VU
Annex II to the SPA/BD Callogorgia verticillata CR Critically Endangered, EN Endangered, VU Vulnerable
protocol Lophelia pertusa Amendment December 2017
a
Madrepora oculata
Antipathella subpinnata
Antipathes dichotoma
damaging these communities would have dramatic conse-
Leiopathes glaberrima
Parantipathes larix quences for the ecosystem.
Reference List of marine Facies of soft muds with Funiculina As a result of the 2016 IUCN assessment, the Decision2 to
habitat types for the quadrangularis and Aporrhais include 3 new deep anthozoans species (I. elongata,
selection of sites to be serresianus Desmophyllum dianthus, Dendrophyllia cornigera) together
included in the National Facies of compact muds with Isidella
Inventories of natural sites elongata with the relatively shallow-water species (Dendrophyllia
of conservation interest Biocenosis of deep-sea corals ramea) in Annex II was adopted at the last Contracting
Habitats Directive/European Union Parties meeting to the Barcelona Convention (December
ANNEX I: Natural habitat 1170 reefs. Examples of habitat 2017) (Fig. 46.1). Despite this, there is an important lack of
types of community forming species included under this
information for other deep-water species and this is particu-
interest whose category:
conservation requires the Callogorgia verticillata
larly evident for the southern and Levantine basin where
designation of special Dendrophyllia cornigera more research would help develop management and conser-
areas of conservation Desmophyllum dianthus vation plans for the entire Mediterranean basin.
Lophelia pertusa At present, very few countries have enacted legislations
Madrepora oculata
aimed at protecting CWC taxa in their waters, and these are
mostly limited to the decisions adopted by the Conference of
species in need of regulation, to more than 40. The Cnidaria Parties, with the exception of the protection of ‘Near
taxa, initially represented only by Gerardia savaglia (Savalia Threatened’ species such as the gold coral S. savaglia, the
savaglia) and Antipathes sp.plur. included in Annex II and gorgonian Callogorgia verticillata or other species of black
by the red coral, Corallium rubrum in Annex III, was further corals (Otero et al. 2016). Endangered species legislation at
updated in 2013 with the inclusion of the following species: national level is also necessary to strengthen protection of
Callogorgia verticillata, Lophelia pertusa, Madrepora ocu- species classified as ‘threatened’, as such legal regulations
lata, Antipathella subpinnata, Leiopathes glaberrima, should aim to control human activities that lead to species
Parantipathes larix and Antipathes dichotoma. This was a declines. Listing species under national legislation should
significant big step forward to improve protection of deep- further trigger actions towards enhancing their protection
sea structuring species, as they had never been considered in status (e.g. recovery plans), enforcement of regulations to
this context. reduce threats and / or identifying habitats for protection.
In 2016, the IUCN regional Red List assessment classi- Likewise, the reference List of Marine Habitat Types
fied several anthozoan species with a deep-water distribution under the Barcelona Convention also aims to assist
as “Threatened” and includes one of them, the bamboo coral Mediterranean countries in the selection of sites to be
Isidella elongata as “Critically Endangered”, mainly as a
result of deep-water bottom trawling (Otero et al. 2017; 2 Draft Decision IG.23/10: Amendments to Annex II to the Protocol
Table 46.2). The available information on the current status concerning Specially Protected Areas and Biological Diversity in the
Mediterranean (UNEP(DEPI)/MED IG.23/13). 20th Ordinary Meeting
of different Mediterranean CWC populations suggest that of the Contracting Parties to the Convention for the Protection of the
similar conditions exist also for other CWC species and that Marine Environment and the Coastal Region of the Mediterranean and
its Protocols. Tirana, Albania, 17–20 December 2017.
Fig. 46.1 Mediterranean
anthozoan species recently
included in Annex II of the
SPA/BD Protocol to the
Barcelona Convention (a)
Isidella elongata; (b)
Desmophyllum dianthus; (c)
Dendrophyllia cornigera; (d)
Dendrophyllia ramea. (Photo
credits (a,b,c) © OCEANA; d
© OCEANA/Carlos
Minguell)
included in the national inventories of Natural Sites of (Van Dover et al. 2014). Thus, prioritisation of conservation
Conservation Interest. This tool is being currently updated3 policies with a more holistic approach that ensures those spe-
to also include deep-sea habitats and will also be reflected in cies and community assemblages identified most at-risk of
activities within the Dark Habitats Action Plan (Action Plan global or regional extinction or those that play important
for the conservation of habitats and species associated with ecological roles should be part of the guiding principles for
seamounts, underwater caves and canyons, aphotic hard beds marine management. Populations of CWCs are especially
and chemo-synthetic phenomena in the Mediterranean Sea, vulnerable because their slow growth rates (Orejas et al.
UNEP-MAP-RAC/SPA 2015). 2008; 2011a, b; Lartaud et al. 2013, 2014, 2017, this volume)
At European level, for Member States (European Union), and frequent patchy distribution (Orejas et al. 2009; Vertino
the biotope formed by CWCs (facies, banks and communi- et al. 2010; Gori et al. 2013; Savini et al. 2014; Chimienti
cates) could be considered4 as “habitat type 1170 Reefs” et al., this volume). These considerations have led to
under Annex I of the EC Habitats Directive 92/43/ enhanced efforts worldwide for the protection of CWC spe-
EEC. Pursuant to this Directive, measures shall be taken by cies and their habitats at international and regional level
Member States to maintain or restore the favourable conser- through their inclusion within biodiversity conservation and
vation status for those habitats listed, as CWCs provide fisheries policies.
important habitat for deep-sea commercial species (fish and Given the existing policy context, increasing numbers of
crustaceans) (Nouar and Maurin 2001; D’Onghia et al. 2010, MPAs have been designated, with few also involving off-
2011, 2012; Baillon et al. 2012; Mastrototaro et al. 2017; shore areas (MedPAN & UNEP-MAP RAC/SPA, in prep).
D’Onghia, this volume), spatial closures to protect CWCs Therefore, the establishment of MPAs in deep waters is how-
may also be a useful tool for the management of those spe- ever very limited. The presence of the framework-forming
cies or the habitat they create (Milligan et al. 2016). species L. pertusa and M. oculata with, among others, soft
Compared with coastal systems, the capacity for recovery corals, sponges, bryozoans and black corals occurs in only a
from human disturbance of deep-sea ecosystems is much few designated MPAs from the western Mediterranean Sea
less understood and recovery rates are thought to be longer such as the National Park of Calanques in France or the
Chella bank (Seco de los Olivos) in Spain, this last one
declared in 2014 as Site of Community Importance (SCI). In
3
See Annex II to Draft Decision IG.23/8 (UNEP(DEPI)/MED addition, it is also worth highlighting that important hard-
IG.23/11): Updated Action Plan for the Conservation of Marine and
bottom communities dominated by millenial colonies of L.
Coastal Bird Species listed in annex II to the Protocol concerning
Specially Protected Areas and Biological Diversity in the Mediterranean. glaberrima as well as soft-bottom communities dominated
Updated Reference List of Marine and Coastal Habitat Types in the by the now rare bamboo coral I. elongata, occur in areas
Mediterranean. 20th Ordinary Meeting of the Contracting Parties to the which remain unprotected (Bo et al. 2015; Mastrototaro
Convention for the Protection of the Marine Environment and the
et al. 2017).
Coastal Region of the Mediterranean and its Protocols. Tirana, Albania,
17–20 December 2017. These few examples provide an idea that overall, the cur-
According to the Interpretation Manual of European Union Habitats
4 rent Mediterranean MPA network offers very limited protec-
(European Commission 2013). tion to CWC habitats, and in turn, to its associated
biodiversity. Despite recommendations made following the see Table 46.3). Criteria for identifying VMEs have not been
2012 MPA status report (Gabrié et al. 2012) about the lack of applied consistently across regions and different approaches
protection for deep-sea areas, no substantial changes have have been used when selecting fauna as indicators, from
been made to address this gap in recent years. While MPAs order or family level to species (FAO 2016a). Considering
and Other Effective area-based Conservation Measures that threshold limits need to be appropriated for the specific
(OECMs) coverage increased from 4.56% (2012) to 7.14% biogeographic region – or sub-region – and the taxa con-
(2016) in the Mediterranean basin, more than 55% of this cerned, the approach to define bycatch thresholds in most of
increment just covers depth ranges between 0–200 meters the RFMOs cases seems to be particularly inadequate to
leaving highly biodiverse deep-sea areas unprotected.5 To ensure conservation of these ecosystems. Thus could be the
counter these deficiencies in spatial coverage, legislative case given the nature of certain deep-sea corals (e.g.
protection for representative populations of these species is Funiculina quadrangularis, I. elongata) with low weights
urgently needed given the current threats and pressures. and elongated or arborescent shape where standard encoun-
From a fisheries perspective, the conservation of CWCs is ter protocols generally set the bycatch limits in weight and at
linked to the protection of vulnerable marine ecosystems such high levels that rules becomes meaningless (Weaver
(VMEs) which has been a legal mandate for Regional et al. 2011) and are likely to have little or no conservation
Fisheries Management Organisations (RFMO) and States value. Thereafter, the designation of closures also varies
since 2008. Specific requirements for that are laid out under depending on the region (see Table 46.4) and may be based
UNGA Resolutions 59/25, 61/105 and 64/72 which FAO on known occurrence of VMEs, predictive modelling, or just
used to develop the International Guidelines for the based on a precautionary approach because of certain geo-
Management of Deep-sea Fisheries (Armstrong et al. 2014). morphological features (e.g. seamounts) where VMEs occurs
These are the basic guidelines to develop and implement fur- or is likely to occur (FAO 2016a).
ther measures (e.g. encounter protocols with associate In addition, with respect to performance, very few
thresholds, closure areas, etc.) in order to ensure protection encounters are usually reported to RFMOs Secretariats,
of certain groups of species and habitats from significant which may indicate: (1) a lack of compliance with the proto-
adverse fisheries impacts at regional and national level. cols; (2) the fact that thresholds have been set too high; or (3)
CWCs (stony corals (Scleractinia), alcyonaceans as result of the protocols or management measures in place,
(Octocorallia), and black corals (Antipatharia) are included fishing vessels actively avoid areas where VMEs might be
among the group of species considered sensitive and poten- encountered. This highlights the further need to refine the
tially vulnerable to deep-sea fisheries and could be initially different approaches, standardise them when suitable, assess
considered as habitat-building species which may contribute their effectiveness and make improvements where needed.
to forming VMEs (FAO 2009). According to the FAO Given the uncertainties about the location of many
Guidelines (paragraph 66), “in areas where VMEs have been Mediterranean VMEs and their resilience, additional mea-
designated, or are known or likely to occur, based on seabed sures such as the employment of onboard scientific observ-
surveys and mapping or other best available information, ers, the identification of VMEs and decision criteria for
States and RFMO/As should close such areas to DSFs until encounters while fishing, the avoidance of bottom-contact
appropriate conservation and management measures have fishing (trawlnets and longlines) in some areas and the delin-
been established to prevent significant adverse impacts on eation of boundaries for VMEs are still on need to be defined
VMEs and ensure long-term conservation and sustainable for the Mediterranean.
use of deep-sea fish stocks”. Following this recommendation, In the Mediterranean context, the General Fisheries
current spatial closures aiming to provide protection for Commission for the Mediterranean (GFCM) is the RFMO in
VMEs are further on need of implementation in certain charge of implementing such measures. While VME proto-
regions (Gianni et al. 2016) including the Mediterranean cols and measures have been already developed and imple-
Sea. mented in other regions globally, the only Mediterranean-wide
More in detail, while general criteria have been produced measure established by GFCM to date with regards to pro-
through the Guidelines (Armstrong et al. 2014) there are no tection of these VMEs is the prohibition of trawling below
protocols that elaborate the procedure, from initial identifica- 1000 m. Such a measure leaves many CWC habitats entirely
tion to the protection of VMEs (Ardron et al. 2014). unprotected knowing the depth-range for most of these spe-
Consequently, implementation of such resolutions varies in cies is 100–600 m. Only three spatial closures for fisheries
terms of approach and performance of management mea- (Fisheries Restricted Areas, FRA) have been established in
sures in place along the different RFMOs (Gianni et al. 2016; order to safeguard deep-sea sensitive habitats and from these,
a single site, “Lophelia reef off Capo Santa Maria di Leuca”
GIS calculation based on MapaMED database, http://www.mapamed.
5 has been reported with CWCs occurrence (see Table 46.4).
org/. Furthermore, weakness in the management and effectiveness
Table 46.3 Implementation approaches for VME protection developed by Regional Fisheries Management Organisations
VME INDICATOR TAXA
RFMO CWCs considered (species/group or
Biogeographic region Taxa level species/habitat) Threshold
NAFOa Family Stony Corals 60 kg of live coral
Northwest Atlantic Gorgonian corals
Sea pens
NEAFCa Family or species CWC reefs >30 kg of live coral
North East Atlantic Coral garden (hard and soft bottoms)
SEAFOa Order or Family Gorgonacea (Order): Gorgonian corals Bottom trawling: 60 kg of live coral
South East Atlantic Anthoathecatae (Family): Hydrocorals Longline: at least 10 VME-indicator units (1
Scleractinia (Order): Stony corals unit = 1 kg or 1 L of live coral) in one 1200 m
Antipatharia (Order): Black corals section of line or 1000 hooks
Zoantharia (Order): Zoanthids Pot set – at least 10 VME-indicator units (1
Alcyonacea (Order): Soft corals unit = 1 kg or 1 L of live coral and/or live sponge) in
Pennatulacea (Order): Sea pens one 1200 m section of line in both existing and new
fishing areas
CCAMLRa Order or Family Gorgonacea (Order) Reporting thresholds >5 units on one line segment
Antartic Anthoathecatae (Order)
Stylasteridae (Family)
Scleractinia (Order)
Antipatharia (Order)
Zoantharia (Order)
SPRFMOa Order Actinaria NO
South Pacific Scleractinia
Antipatharia
Alcyonacea
Gorgonacea
Pennatulacea
GFCMb Order Hexacorallia (Antipatharia, Scleractinia) Not defined yet
Mediterranean* Octocorallia (Alcyonacea, Pennatulacea)
Based on Weaver et al. (2011), Gianni et al. (2016) and RFMOs
*As adopted at the 42nd session of the GFCM Commission (2018)
a
Move-on rule in place
b
No move-on rule in place
Table 46.4 Closure areas in place by RFMO

RFMO
Biogeographic region Closure areas for VME protection
NAFO 6 Seamounts: Fogo Seamounts 1; Fogo Seamounts 2; Orphan Knoll; Corner Seamounts; Newfoundland
Northwest Atlantic Seamounts; New England Seamounts
1 Coral Area Closure
9 High Sponge and Coral Concentration Area Closures: Tail of the Bank; Flemish Pass/Eastern Canyon; Beothuk
Knoll; Eastern Flemish Cap; Northeast Flemish Cap; Sackville Spur; Northern Flemish Cap; Northwest Flemish
Cap; Beothuk Knoll
NEAFC 13 Seamounts: Northern, Middle (Charlie-Gibbs Fracture Zone and sub-Polar Region) and Southern Mid-
North East Atlantic Atlantic-ridge (MAR); Altair Seamount; Antialtair Seamount; Hatton Bank 1 and 2; Rockall Bank; Logachev
Mounds; West Rockall Mounds; Edora’s bank; Southwest Rockall Bank; Hatton-Rockall Basin
SEAFO 12 Seamounts: Unnamed seamount; Kreps seamount; Malachit Guyot Seamount; Wüst seamount; Africana
South East Atlantic seamount; Schmidt-Ott Seamount; Unnamed; Vema Seamount; Herdman Seamounts; Unnamed Seamounts;
Unnamed Seamounts; Valdivia Bank South (pots and longlines allowed)
CCAMLR 46 identified VME areas (of these, 42 VMEs are in areas where bottom fishing is currently prohibited; in the
Antartic remaining 4, toothfish fisheries are permitted and are afforded specific protection)
SPRFMO 20 areas in New Zealand
South Pacific No one in Australia
GFCM Eratosthenes seamount; Santa Maria di Leuca (CWC reefs); Nile delta (cold seeps. Jabuka/Pomo Pit (mud
Mediterranean volcanoes, pockmarks, sea pen fields, oyster beds)
Based on Weaver et al. (2011), Gianni et al. (2016), FAO (2016a), and RFMOs
of these fisheries restricted areas (FRA) has also been Within these aforementioned overarching policies and
reported (GFCM 2014). strategies, significant challenges remain as how to achieve
Discussions at the Mediterranean level for the implemen- and properly regulate the economic outcomes from the “Blue
tation of management measures to enhance conservation of economy” while mitigating the negative impact of certain
VMEs (including CWCs) are now ongoing under the newly economic activities in the open seas of the Mediterranean
established GFCM Working Group of Vulnerable Marine basin. CWCs are likely to be significantly impacted by these
Ecosystems (WGVME April 2017). Future works should policies and their resulting anthropogenic activities.
continue on this line, defining appropriate encounter proto- Climate change including OA will further put at risk
cols with associated move-on rules, impact assessments and deep-sea communities in the near future (see chapters by
developing management measures in areas where a VME Maier et al., this volume; Movilla, this volume). Incorporating
encounter has been reported or VMEs are likely to exist climate change projections into conservation planning for
according to FAO Deep-sea Guidelines (FAO 2016b). CWCs are essential components for future efforts in the
Mediterranean Sea. This could be used for example to iden-
tify locations for MPAs or FRAs where CWCs are less likely
46.4 F
uture Perspectives for Conservation to be affected by climatic disturbances while facilitating, at
Planning and Good Governance the same time, connectivity among populations to enhance
their resilience. A possible example could be made by explor-
With the realisation of the economic value of the coastal and ing the protection through a network of deep-sea MPAs or
open seas, the concept of sustainable development linked to FRAs covering the know distribution of the important sites
the “Blue Growth” EU strategy is becoming of increased for living white corals frameworks (dominated by Madrepora
importance in the development of policies and instruments in oculata). These sites located in the South-western Adriatic
the Mediterranean Sea. The Blue Growth (BG) agenda pro- Sea, northern Ionian Sea, Strait of Sicily, the Gulf of Lion,
mulgated by the European Commission (2012) is seen as an the westwards to Alborán Sea and off Sardinia, seem to cor-
ambitious framework for ocean management within EU respond to the core water flux of the Levantine Intermediate
waters, seeking to foster a more coherent approach to mari- Water (LIW) which possibly acts as a vector for larval dis-
time issues and the growth of marine economic sectors (blue persal thus connecting disjoint CWC areas in the
energy, aquaculture, maritime, coastal and cruise tourism, Mediterranean Sea (Taviani et al. 2017; Chimienti et al., this
marine mineral resources, and blue biotechnology). This fur- volume). Similar approaches could be explored with pristine
ther requires appropriate management measures to ensure and unique black coral gardens, the now rare bamboo coral
environmental sustainability and good environmental status Isidella elongata, and other longevous and rare coral species
(GES) in line with the Marine Strategy Framework Directive6 (e.g. Bo et al. 2015; Mastrototaro et al. 2017; Bo and
(MSFD). At the broader regional scale, within the Barcelona Bavestrello, this volume; Chimienti et al., this volume).
Convention, the Mediterranean Strategy for Sustainable Configure an MPA network that enhances connectivity of
Development (MSSD) has also formulated a similar agenda these key habitats while furthermore estimating and assess-
for the period 2016–2025. This framework embeds the need ing the timescale and distances over which climate change
for BG and the increase in the exploration for, and exploita- impacts will be expected, will mitigate these effects and
tion of, non-living open sea resources. This effort would be assist to establish ecological linkages and pathways for a
directed to establishing and enforcing regulatory mecha- wide range of species.
nisms, including Maritime Spatial Planning (MSP), to pre- Moreover, good governance is still underdeveloped for
vent and control unsustainable open ocean resource managing Mediterranean Sea affairs. The involvement of
exploitation as well as support sustainable development. stakeholders with an interest in the deep-sea (governments,
From fisheries perspective, the GFCM has developed and members of industry, academic world, intergovernmental
adopted the Mid-Term Strategy 2017–2020 towards the sus- panels, NGOs) will likely evolve and expand as human activ-
tainability of Mediterranean and Black Sea fisheries. This ities increase. Mechanisms that promote this participation
strategy is based on five targets, one of them (Target 4) aim- and multi-stakeholder engagement, e.g., national and inter-
ing to “minimize and mitigate unwanted interactions between national governance frameworks, corporate responsibility or
fisheries and marine ecosystems and environment”. voluntary code of conduct, could be effective means to share
tools and to make collective decisions that ensures conserva-
tion as well as adequate, viable, and long-term management
measures.
Directive 2008/56/EC of the European Parliament and of the Council
6
of 17 June 2008 establishing a framework for community action in the

Additional scientific studies are also essential to have a
field of marine environmental policy (Marine Strategy Framework more comprehensive census and understand the distribution
Directive). of CWCs and their assemblages. This information represents
a tool to legislate and manage the marine environment in a (Mediterranean Sea): observations and conservation straits.
Deep-Sea Res Part 2 Top Stud Oceanogr 145:87–101. https://doi.
sustainable manner. Collectively these measures could have org/10.1016/j.dsr2.2016.02.012
a considerable impact on conservation and management Danovaro R, Dell’Anno A, Pusceddu A (2004) Biodiversity response to
efforts ensuring a more dynamic approach to safeguard climate change in a warm deep sea. Ecol Lett 7:821–828
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for ecosystem-based management of the deep sea. Deep-Sea Res
Acknowledgements We sincerely thank our reviewers (David Johnson Part 2 Top Stud Oceanogr 145:102–109. https://doi.org/10.1016/j.
and Marzia Bo) and the editors (Covadonga Orejas and Carlos Jiménez) dsr2.2017.04.014
of this compilation for their constructive comments on the manuscript DeLeo DM, Ruiz-Ramos DV, Baums IB, et al (2016) Response of deep-
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net/10013/epic.37995
Species Index
A Anthias
Abra longicallus, 305, 318 A. anthias, 338, 348
Acanella A. woodsi, 342, 348
A. arbuscula, 128, 141, 149, 150, 536 Anthomastus sp., 127, 138, 141, 143, 149, 302, 316
A. furcata, 128, 141, 150 Antho
Acanthephyra eximia, 306 A. involvens, 299, 313
Acantheurypon pilosella, 299, 313 A. signata, 299, 313
Acanthogorgia sp., spp., 138, 320, 345, 438 Antipathella sp., spp., 131, 341, 453
A. armata, 128, 142, 143, 149, 302, 341, 453 A. subpinnata, 125, 126, 130, 131, 160, 222–224, 228, 246, 247,
A. hirsuta, 128, 142, 143, 160, 161, 220, 231, 246, 253, 302, 315, 249, 250, 301, 338, 427, 450, 538
321, 337, 338, 453 A.wollastoni, 125, 249
Acantholabrus palloni, 310, 325 Antipathes sp., 196, 345, 349, 538
Acartia sp., 306 A. aenea, 131
Acesta excavata, 19, 21, 296, 305, 312, 314, 316, 318 A. dichotoma, 125, 126, 130, 131, 160, 161, 180, 214–216,
Acropora millepora, 379, 382, 490 222–225, 227–229, 246, 247, 249, 250, 301, 315, 338, 348,
Acryptolaria 451, 453, 538
A. conferta, 301, 317 A. fragilis, 125, 126, 130, 131, 249
A. crassicaulis, 301, 317 A. gracilis, 131
Aetea Apionsoma murinae bilobatae, 305
A. sica, 308 Apogon queketti, 514
A. truncata, 308 Apristurus
Aglaophamus cf. elamellatus, 303 A. brunneus, 345, 349
Aglaophenia tubulifera, 301, 317 A. profundorum, 345, 349
Albatrossia pectoralis, 344, 349 Arctozenus risso, 310
Alcyonium sp., spp., 139–141, 162, 450 Aricidea
A. acaule, 127, 141 A. cf. pseudoarticulata, 303
A. coralloides, 127, 141 A. simonae, 303
A. palmatum, 127, 141, 258, 453 Aristaeomorpha foliacea, 232, 306, 320
Alectona millari, 299 Aristeus antennatus, 232, 293, 306, 312, 320
Allocareproctus unangas, 345, 349 Artemia sp., 444, 451, 452, 462
Alvania A. salina, 416, 450–453, 456
A. cimicoides, 305 Asconema setubalense, 160–163, 263, 300, 313, 314, 326
A. testae, 305 Asperarca nodulosa, 110, 296, 305, 312, 316, 318
Amphianthus dohrni, 301, 315, 316 Aspidosiphon muelleri muelleri, 305
Amphiblestrum ruggeroi, 308 Astarte sulcata, 305
Amphiura filiformis, 307, 320, 322 Astrospartus mediterraneus, 162, 307, 322
Anamathia rissoana, 306, 320, 321, 339 Atheresthes stomias, 344
Anarhichas lupus, 340, 348 Aulopus filamentosus, 310, 326
Anatoma tenuis, 305 Axinella
Anchialina agilis, 307 A. cannabina, 299, 313
Anekes sculpturata, 305, 319 A. pumila, 299, 313
Anguisia verrucosa, 309
Anisocrella hymedesmina, 299, 313
Anomocora fecunda, 126, 133, 135, 137, 149 B
Antalis agilis, 306, 318 Babelomurex sentix, 305, 316, 319
Antennella secundaria, 301 Bacteroidetes, 380, 381, 383

https://doi.org/10.1007/978-3-319-91608-8
548 Species Index
Bairdoppilata conformis, 309, 319 Charybdis longicollis, 514

Balanophyllia cellulosa, 18, 126, 133, 135–137 Chaunax stigmaeus, 342
Baldwinella vivanus, 341, 345, 348, 349 Chelonaplysilla psammophila, 299
Bathyarca philippiana, 305, 318 Chimaera monstrosa, 310, 340, 341
Bathynectes maravigna, 306, 320 Chironephthya mediterranea, 127, 141, 143, 149, 162, 536
Bathypterois dubius, 310 Chlorophthalmus agassizi, 310
Bathyvermilia eliasoni, 303 Cidaris cidaris, 161, 217, 220, 307, 314, 320–322, 326
Bebryce, 140 Cirsonella romettensis, 305, 319
B. mollis, 128, 142, 143, 231, 246, 302, 315, 338 Cladocarpus sinuosus, 301, 317
Bedotella armata, 301, 317 Cladocora
Benthocometes robustus, 194, 310, 325, 338, 339, 341, 348 C. caespitosa, 92, 100, 101
Benthosema glaciale, 345, 349 C. debilis, 127, 132, 134, 136, 137
Beringraja binoculata, 344 Clathria
Beryx decadactylus, 342, 348, 350 C. anchorata, 299, 313
Biemna C. frogeti, 299
B. partenopea, 299, 313 C. gradalis, 299
B. tenuisigma, 299, 313 Clavularia, 143
Bispira sp., 303 C. carpediem, 129, 149
Bonellia sp., 303 C. marioni, 129, 143
B. viridis, 303, 318 C. viridis, 143
Brama brama, 310 Cliona sp., 299
Brissopsis atlantica mediterranea, 307, 320 Clytia
Brosme brosme, 340, 343, 348, 350 C. gracilis, 301, 317
Bubaris C. linearis, 301, 317
B. carcisis, 299 Coelorinchus caelorhincus, 310, 337, 341, 348
B. subtyla, 299, 313 Coenocyathus, sp., 135
B. vermiculata, 299 C. anthophyllites, 126, 133, 135
Buskea dichotoma, 308 C. cylindricus, 126, 133, 135
Bythaelurus canescens, 346, 349 Conger
Bythocypris obtusata, 307, 319 C. conger, 220, 310, 311, 325, 326, 337–339, 348–350
C. oceanicus, 325, 342, 344, 348–350
Copidozoum
C C. balgimae, 308
Calanus helgolandicus, 306, 319 C. exiguum, 308, 323, 324
Callogorgia verticillata, 128, 136, 139–141, 143, 161, 162, 180, C. planum, 308
213–220, 222–225, 229–231, 246, 253, 254, 262–263, 302, C. tenuirostre, 308
311, 326, 338, 341, 347, 348, 427, 453, 538 Coralliophaga lithophagella, 305, 319
Callopora dumerilii, 308 Coralliophila
Callostracon thyrrenicum, 305 C. richardi, 21, 305, 312, 316, 319, 327
Calthropella pathologica, 299, 313 C. squamosa, 263, 305, 316, 319
Campanularia hincksii, 301, 317 Corallium rubrum, 7, 52, 129, 138, 140, 143, 218–220, 245, 246, 253,
Capros aper, 310, 337, 338, 348 254, 272, 280, 292, 302, 311, 315, 338, 413, 423, 425–431,
Caryophyllia sp., spp., 16, 18, 48, 52, 74, 91–93, 115, 132, 135, 149, 441, 486–488, 513, 515, 538
262, 318, 324, 344, 398, 399 Coronellina fagei, 308
C. ambrosia, 132 Coryphaena hippurus, 310
C. atlantica, 132 Crassimarginatella crassimarginata, 308
C. calveri, 68, 70, 72, 78, 85–87, 90–92, 126, 133, 137, 259, 301, Crella alba, 299
315, 316 Crellastrina alecto, 299, 313
C. clavus, 135 Crepis harmelini, 308, 323
C. communis, 76 Crisia
C. coronata, 52, 68, 70, 72, 75, 77–79 C. ramosa, 309
C. cyathus, 75, 126, 133, 137, 301, 311, 323 C. sigmoidea, 309
C. inornata, 123, 126, 132, 133, 301 C. tenella, 309
C. sarsiae, 19, 22, 52, 68, 70, 72, 77, 85–87, 132 Crispatotrochus rugosus, 132
C. smithii, 19, 85–87, 90, 92, 101, 126, 133, 135, 136, 292, 301, Cryptolaria pectinata, 301, 317
311, 394, 520–522 Cyclopecten hoskynsi, 305
Cavernularia pusilla, 129, 145–147, 302
Cellaria salicornioides, 308
Centropages sp., 306 D
Centrophorus granulosus, 310, 337 Dalatias licha, 310, 337
Centropristis striata, 341, 345, 348–350 Damiria curvata, 299
Cepola macrophthalma, 338, 348 Daniela koreni, 141, 150
Ceratocyathus, 52 Danilia tinei, 305, 316, 318
Ceratotrochus magnaghii, 126, 132, 133 Dasyatis centroura, 345, 349
Cerithium sp., 466, 467 Deania calcea, 341
Chaetaster longipes, 308 Delectopecten vitreus, 21, 22, 305, 312, 316, 318
Characella pachastrelloides, 299, 313, 315 Deltaproteobacteria, 380, 381, 383
Species Index 549
Deltocyathus, 52, 74, 149 Epizoanthus sp., 302

Dendrobrachia bonsai, 128, 142, 143, 149, 253, 254, 302, 536 Eptatretus lopheliae, 342, 348, 350
Dendrophyllia sp., spp., 48, 54, 67, 68, 74, 75, 91, 135, 228, 257–259, Errina aspera, 52, 130, 148, 150, 214, 215, 221, 222, 225,
319, 394, 418 231–232, 237
D. alternata, 68, 341 Erylus
D. cornigera, 16, 19, 53, 68, 74, 75, 77, 85–87, 90, 92, 93, 123, E. discophorus, 299
127, 132, 133, 135, 136, 160–162, 214–225, 228–230, 257, E. papulifer, 299, 313
262, 263, 271–273, 280, 286, 287, 291–293, 297, 302, 311, Escharella
313, 315–317, 319, 322, 324, 326, 392–397, 407, 411, 413, E. acuta, 308
415, 417, 418, 439, 444, 445, 450, 451, 454, 456, 457, 463, E. longicollis, 308
515, 520–523, 525, 531, 532, 538, 539 E. octodentata, 308
D. ramea, 7, 127, 133, 135, 136, 161, 228, 257–259, 297, 322, E. ventricosa, 308, 323
394, 396, 397, 444, 445, 466, 515, 536, 538, 539 Escharina
Dercitus plicatus, 299 E. dutertrei protecta, 308, 323
Desmacella E. vulgaris, 259, 308, 323
D. annexa, 299, 315 Esperiopsis strongylophora, 299
D. inornata, 299, 313, 315 Etmopterus spinax, 311, 325, 337, 338, 348, 349
Desmophyllum sp., spp., 19, 21, 22, 24, 32, 48, 74, 75, 77–79, 87, 115, Eunice sp., spp., 19, 22, 303
135, 140, 196, 322, 323, 388 E. dubitata, 303
D. dianthus, 6–8, 16, 18–23, 31, 32, 41, 42, 68, 70, 72, 74, 75, 77, E. norvegica, 11, 263, 298, 303, 312, 316–318, 327, 367–368, 407,
79, 85–93, 95–97, 101, 103, 104, 126, 132, 133, 135, 193, 408, 416, 460
214–227, 271–273, 276–281, 297, 302, 311, 314–316, 321, Eunicella sp., spp., 139–142
324, 337, 357, 358, 363–368, 373–375, 392–398, 409–415, E. cavolini, 128, 141, 143, 162, 245, 246, 292, 302, 347,
418, 444, 450, 451, 456, 462–464, 486, 487, 489, 515, 517, 453, 487
520–525, 531–533, 538, 539 E. filiformis, 128, 142, 143
D. pertusum, 11, 71, 135, 221, 368, 374, 407 E. singularis, 124, 128, 141, 245, 246, 453, 487
Diaixis pygmaea, 306, 319 E. verrucosa, 128, 141–143, 161, 162, 247, 302, 450
Diphasia margareta, 301, 317 Eurypon
Dipturus oxyrinchus, 310 E. cinctum, 299, 313
Distansescharella alcicornis, 308 E. clavatum, 299
Dodecaceria sp., 303 E. denisae, 299
Dragmatella aberrans, 299 E. hispidulum, 299
Dysommina rugosa, 342, 348 E. obtusum, 299
E. topsenti, 299, 313
E. viride, 299
E Euthynnus alletteratus, 341
Ebalia sp., 306 Evagora rosea, 143
E. nux, 306, 320 Exidmonea
Echinus melo, 307, 320, 322 E. coerulea, 309
Eclysippe sp., 303 E. flexuosa, 309
Edwardsiella loveni, 302, 315 Exogone sp., 303
Eguchipsammia, 149
E. cornucopia, 53, 68
E. fistula, 418 F
E. gaditana, 302 Farrea sp., 300, 313
Ellisella paraplexauroides, 128, 142, 162, 453 Fauveliopsis sp., 303
Emarginula, 319 Fenestraja plutonia, 345, 349
E. adriatica, 305 Fenestrulina malusii, 308
E. multistriata, 305 Filigorgia guineensis, 128, 142, 143, 149
E. tenera, 305 Filograna sp., 303
Enallopsammia sp., 19, 48, 74, 79, 150 F. implexa, 303, 318
E. rostrata, 52, 68, 70, 398, 399, 414, 486 Filogranula
E. scillae, 18–20, 52, 68–70, 74, 75, 77–79 F. annulata, 303
Endozoicomonas, 378, 382, 383 F. gracilis, 303, 317
Ennucula aegeensis, 305, 318 F. stellata, 22, 303
Entalophoroecia Flabellum sp., spp., 48, 52, 74, 76, 149, 150, 262, 318, 398, 399
E. deflexa, 309 F. alabastrum, 19
E. robusta, 309 F. chunii, 302, 311, 315, 316
Epigonus constanciae, 310 F. impensum, 100
Epinephelus spp., 341 F. macandrewi, 53
E. drummondhayi, 341, 345, 348–350 Fungiacyathus sp., 52, 149, 150, 398
E. itajara, 341, 348 F. marenzelleri, 398
E. morio, 341, 348 Funiculina quadrangularis, 129, 145–147, 213–215,
Epitonium 218, 219, 222–225, 232, 234, 235, 302, 315, 316,
E. algerianum, 305, 316, 319 538, 540
E. celesti, 305, 319 Fusinus rostratus, 305
550 Species Index
G Hirtomurex (=Coralliophila) squamosa, 263

Gadella maraldi, 310 Holophaga acidobacteria, 382
Gadus Holothuria
G. chalcogrammus, 344, 349 H. forskali, 277, 280, 307, 322
G. macrocephalus, 344, 349 H. tubulosa, 307, 322
G. morhua, 340, 343, 348 Homola barbata, 306, 320
Galathowenia oculata, 303 Hoplangia durotrix, 126, 133
Galeocerdo cuvieri, 341 Hoplostethus
Galeus melastomus, 311, 325, 326, 337–341, 343, 345, 348–350 H. mediterraneus, 310, 325, 326, 337–339, 348
Geodia H. occidentalis, 342, 348
G. anceps, 299, 313 Hyalopomatus
G. nodastrella, 299 H. madreporae, 303, 317
Gephyroberyx darwini, 342, 348 H. variorugosus, 303
Geryon longipes, 306, 320 Hybocodon cf. prolifer, 301, 317
Glycera tesselata, 303 Hymedesmia
Gnathia sp., 307 H. gracilisigma, 300
Goniocorella dumosa, 398, 486 H. inflata, 300
Gonioinfradens H. mutabilis, 300
G. giardi, 514 H. plicata, 300
G. paucidentatus, 514 H. pugio, 300
Gorgonia profunda, 143 H. serrulata, 300
Gracilechinus acutus, 307, 320, 322 Hymenocephalus italicus, 310
Grammicolepis brachiusculus, 342, 348 Hymerhabdia
Gregarinidra gregaria, 308 H. oxytrunca, 300
Gryphus vitreus, 22, 309, 324 H. typica, 300, 313
Guttigadus latifrons, 340, 348 Hyperoglyphe perciformis, 342, 348
Guynia annulata, 85, 86, 88, 90–92, 127, 132, 134–136 Hyporthodus
H. nigritus, 341, 348
H. niveatus, 341, 342, 345, 348–350
H
Hacelia superba, 308, 322
Halecium labrosum, 301, 317 I
Haliclona Idiastion kyphos, 342, 348
H. arnesenae, 299 Inachus leptochirus, 307
H. magna, 299 Iphimedia obesa, 306
H. mucosa, 299, 313 Iphitus tuberatus, 305, 316, 319, 327
Halopteris catharina, 301, 317 Isidella elongata, 52, 121, 128, 139, 141, 143, 161, 213–215, 219,
Hamacantha 220, 222–225, 232–234, 246, 247, 298, 302, 311, 312, 315,
H. azorica, 299, 313 316, 320, 325, 338, 339, 347–349, 427, 476, 477, 536,
H. falcula, 161, 299 538–540, 542
H. johnsoni, 299 Isozoanthus primnoidus, 302, 316
H. lundbecki, 299
H. papillata, 299, 313
Haplopoma sciaphilum, 308, 323 J
Haplosyllis Janita fimbriata, 303
H. chamaeleon, 303, 318 Janulum spinispiculum, 300, 313
H. spongicola, 303 Jaspis incrustans, 300, 315
Harmothoe Javania cailleti, 16, 18, 22, 85, 86, 88, 92, 127, 134, 135, 137
H. cf. evei, 303 Jaxea nocturna, 307
H. vesiculosa, 303, 318
Harpinia dellavallei, 306
Helicolenus dactylopterus, 220, 310, 311, 325, 337–343, 348–350 K
Helmutneris flabellicola, 303, 316 Kadophellia bathyalis, 302, 315
Herentia hyndmanni, 308, 322–324 Karnecampia sulcata, 305, 318
Heteranomia squamula, 305, 306, 312, 318 Kelliella miliaris, 305
Heterosaccus dollfusi, 514 Kophobelemnon sp., 262
Hexadella K. leuckartii, 129, 147
H. cf. cripta, 300 K. stelliferum, 129, 145–147, 161, 213–216, 219, 220, 222–225,
H. dedritifera, 300, 313, 388 234, 235, 302, 315
H. pruvoti, 300, 313
Hexanchus griseus, 311, 337, 341, 343, 348
Hiatella arctica, 305 L
Higginsia thielei, 388 Laemonema
Hincksina longispinosa, 308, 324 L. barbatulum, 342, 348
Hippomenella mucronelliformis, 308 L. goodebeanorum, 342, 348
Hippothoa flagellum, 308 L. melanurum, 342, 348
Species Index 551
Lafoea dumosa, 301 127, 132, 134, 136, 137, 157, 161, 164, 165, 179, 193, 194,
Lanice conchilega, 303 213–228, 253, 254, 262, 263, 265, 266, 271–273, 278–281,
Laodicea undulata, 301, 317 286, 287, 291–293, 296–298, 302, 311, 313–315, 317,
Lappanella fasciata, 338, 341, 348 319–326, 337, 339–342, 347–349, 357–363, 365, 366, 368,
Latrunculia rugosa, 300 377–384, 387–389, 392–399, 407, 408, 411–418, 427, 431,
Ledella messanensis, 306, 318 437, 441, 444, 450, 451, 456, 463, 486, 487, 489, 500, 515,
Leiochrides sp., 303 517, 520–525, 531, 532, 538, 539, 542
Leiodermatium cf. lynceus, 300, 315 Magelona wilsoni, 304
Leiopathes glaberrima, 121, 125, 126, 130, 131, 161, 164–166, 180, Malacocephalus occidentalis, 343, 348
213–220, 222–225, 227–229, 246, 247, 249–251, 253, 254, Manta birostris, 341
297, 302, 311, 314–316, 322, 325, 326, 338, 339, 347–349, Mathilda cochlaeformis, 305
413, 427, 428, 431, 451, 453, 538, 539 Megabalanus tulipiformis, 306, 320
Leitoscoloplos mammosus, 303 Megathiris detruncata, 309, 324
Leocrates atlanticus, 303 Megerlia truncata, 22, 309, 324, 325
Lepidion sp., 343 Melonanchora emphysema, 300
L. eques, 340, 341, 348 Melphidippella macra, 306, 319
L. lepidion, 310 Merluccius merluccius, 310, 325, 337–339, 348–350
Lepidopus caudatus, 310, 325, 338 Mesothuria intestinalis, 307, 320
Lepidorhombus sp. Metavermilia multicristata, 296, 304, 317
L. boscii, 338, 348 Metaverruca recta, 306, 320
L. whiffiagonis, 310 Micromesistius poutassou, 310, 325, 337, 338, 348, 349
Leptogorgia sarmentosa, 124, 128, 142, 143, 161, 245, 247, 338, 450 Mitrella pallaryi, 305, 318
Leptometra phalangium, 308, 321, 322 Mitrocoma annae, 301, 317
Leptomysis gracilis, 307 Modeeria rotunda, 301, 317
Leptopsammia pruvoti, 127, 132, 134, 135 Mola mola, 341
Leucoraja sp. Mollia patellaria, 308
L. circularis, 311 Molva
L. fullonica, 311 M. dipterygia, 310
Lima marioni, 306, 318 M. molva, 340, 348
Limea crassa, 306 Monodaeus couchii, 307, 320
Limopsis aurita, 306 Monomyces pygmaea, 127, 132, 134, 135
Lissotesta turrita, 305, 319 Mora moro, 310, 341, 343, 348
Lophelia pertusa, 5, 6, 8–11, 16, 18–20, 31, 32, 41, 42, 52, 53, 57–60, Munida sp., spp., 193, 277, 280, 292, 307, 319, 321, 340, 350
62, 67–79, 85, 86, 88, 89, 91–93, 95, 98–101, 116, 121, 126, M. intermedia, 307, 320
132, 133, 135–137, 140, 157, 160, 161, 164, 165, 193, M. tenuimana, 307, 320
213–228, 253, 254, 263, 265, 266, 271–273, 278–281, 286, Muriceides lepida, 128, 142–143, 162, 218, 231, 253
291, 293, 296–298, 302, 311–315, 317–321, 323, 324, 326, Mycoplasma spp., 379, 380, 382
335, 337, 340–344, 347–349, 357–363, 365, 367, 368, 374, Mycteroperca spp., 341, 350
377–384, 387–389, 392–399, 407–418, 427, 436, 437, M. microlepis, 341, 345, 348–350
439–441, 444, 447, 448, 450–452, 456, 457, 459–463, 465, M. phenax, 341, 345, 348–350
485–492, 500, 515, 517, 520–525, 531, 532, 538, 539 Myriapora truncata, 308
Lophiodes Mysis sp., 445, 451
L. beroe, 342 M. relicta, 450, 451
L. monodi, 342
Lophius piscatorious, 341
Lophogaster typicus, 307, 319 N
Lumbrineriopsis paradoxa, 304 Nassarius lima, 305
Lumbrineris sp., 304 Nemertesia spp., 148
L. latreilli, 304 N. antennina, 301, 317
Lutjanus N. falcicula, 301, 317
L. campechanus, 341, 348 N. ramosa, 301, 317
L. griseus, 341, 348 Nemipterus randalli, 514
Lycodes Neocyttus helgae, 340, 341, 348
L. esmarkii, 345, 349 Neolagenipora eximia, 308
L. vahli, 340, 348 Neopycnodonte sp., 91
Lycopodina hypogea, 194, 300, 313, 315 N. cochlear, 292, 306
Lysidice ninetta, 304 N. zibrowii, 19, 24, 194, 218, 306, 315, 318
Lysippe cf. fragilis, 304 Neovermilia falcigera, 22
Lytocarpia myriophyllum, 301, 317 Nephrops norvegicus, 232
Nephtys cf. paradoxa, 304
Nettastoma melanorum, 343, 348
M Nezumia
Macropipus tuberculatus, 307 N. aequalis, 310
Macroramphosus scolopax, 310, 325, 326, 338, 348 N. sclerorhynchus, 310, 325, 342, 348
Madrepora oculata, 5–8, 11, 16, 18–20, 24, 31, 32, 41, 42, 49, 53, Nicella granifera, 128, 149
57–60, 62, 68, 69, 72–79, 85, 86, 88–93, 95, 100, 110, 121, Nidalia studeri, 127, 141, 143, 150, 453, 536
552 Species Index
Nodastrella nodastrella, 300 Philocheras bispinosus, 307

Normanion ruffoi, 306, 319 Pholoe sp., 304
Notacanthus bonaparte, 310 Pholoides dorsipapillatus, 304
Nothria conchylega, 304 Phycis
Notomastus sp., 304 P. blennoides, 310, 325, 326, 337, 338, 341, 343, 348–350
Novocrania sp., 310, 324 P. phycis, 338, 348
N. anomala, 22, 310, 324 Phyllodoce
Nyctiphanes couchii, 307, 319 P. cf. maculata, 304
P. madeirensis, 304
P. mucosa, 304
O Pionosyllis nidrosiensis, 304
Oculina sp., 48, 74, 341, 345 Placogorgia spp., 129, 139, 140, 150, 231, 303
O. arbuscula, 395 P. coronata, 129, 143, 149
O. varicosa, 335, 341, 345, 348, 349, 398, 399, 414, 448, 451–452, P. massiliensis, 129, 143, 149, 253
461, 486–488 Placostegus tridentatus, 259, 304
Odontaster sp., 308 Plagioecia
O. mediterraneus, 308, 320 P. inoedificata, 309
Oithonak sp., 306 P. patina, 309
Onychocella marioni, 308 Plakina monolopha, 301
Onychoteuthis banksii, 306 Plakortis simplex, 301
Oopsacas minuta, 300 Platidia sp., 309, 324
Ophiothrix sp., 160, 161, 292, 308, 321, 322, 326 Platyscelus ovoides, 306
O. fragilis, 307, 322 Plesionika sp., 307
O. quinquemaculata, 308, 320, 322 P. acanthonotus, 307
P. cf. gigliolii, 307
P. heterocarpus, 307, 320
P P. martia, 307, 312, 320
Pachastrella monilifera, 161, 162, 179, 300, 311, 313 Pleurogrammus monopterygius, 344, 349
Pachylasma giganteum, 19, 219, 306, 320 Pleuromamma sp., 306
Pagellus bogaraveo, 310, 311, 325, 326, 337–339, 347–350 Pleurotomella demosia, 305
Pagodula echinata, 305, 318 Plexauridae spp., 124, 128, 142, 150, 303
Pagrus pagrus, 341 Plocamionida ambigua, 300
Palinurus Podospongia lovenii, 300
P. elephas, 292 Poecillastra compressa, 162, 164, 300, 313, 315
P. mauritanicus, 307, 320, 321 Poecilochaetus sp., 304
Palmiskenea Pollachius virens, 340, 348
P. gautieri, 308 Polycheles typhlops, 307, 320
P. skenei, 309 Polymastia polytylota, 300
Paracyathus pulchellus, 85, 86, 89–92, 126, 132, 133 Polyplumaria flabellata, 301, 314, 317
Paradiopatra hispanica, 304 Polyprion americanus, 310, 325, 337–339, 342, 348
Paralcyonium spinulosum, 127, 141, 143, 453 Porella minuta, 309, 323
Paramuricea sp., 129, 141, 150, 320, 388 Pourtalosmilia anthophyllites, 126, 133
P. clavata, 124, 128, 137, 140–143, 161, 162, 193, 219, 220, 245, Primnoa ellisii, 143
246, 250, 302, 311, 338, 426, 429, 453 Primno sp., 306
P. macrospina, 129, 140, 141, 143, 231, 245, 246, 253, 254, 302, Prionace glauca, 311
319, 338, 453, 487 Prionospio sp., 304
Parantipathes larix, 121, 125, 126, 130, 131, 161, 213–215, 220, Proprionibacterium, 382
222–224, 227–229, 246, 247, 249, 250, 302, 315, 338, 347, Prosuberites longispinus, 300, 313
348, 427, 538 Protanthea simplex, 302, 315
Paraphoxus oculatus, 306 Protoptilum carpenteri, 129, 145–147, 149, 234
Parasabella sp., 304 Protula sp., 304
Parastichopus regalis, 307, 320, 322 P. tubularia, 304
Parazoanthus anguicomus, 302 Pseudotrachya hystrix, 300
Pareurythoe borealis, 304 Psolidium complanatum, 307, 320, 322
Parmaturus xaniurus, 345, 349 Pteroctopus tetracirrhus, 306, 319
Paromola cuvieri, 307, 320 Pteroeides spinosum, 129, 145–147, 234, 538
Peachia cylindrica, 302, 315 Pterois
Peltaster placenta, 308, 322 P. miles, 259, 514
Penares euastrum, 300, 313 P. volitans, 514
Pennatula sp., 144, 147 Pteroplatytrygon violacea, 311
P. aculeata, 129, 144–147, 345, 349 Puellina
P. phosphorea, 129, 144–147, 220, 235, 302, 538 P. hincksi, 259
P. rubra, 129, 144–147, 234 P. pedunculata, 259, 323
Perrierella audouiniana, 306 P. scripta, 309, 323
Petrosia sp., 161, 263, 300, 313 P. setosa, 309
Phakellia robusta, 300 P. venusta, 322
Phalacostemma sp., 304 Putzeysia wiseri, 305, 318
Species Index 553
R Sebastolobus alascanus, 344, 349

Racemoramus panicula, 301 Semivermilia agglutinata, 304
Radicipes challengeri, 149 Seriola
Reteporella sparteli, 309 S. dumerili, 341
Rhabdeurypon spinosum, 300 S. rivoliana, 341
Rhizaxinella pyrifera, 300 Serpula
Rocellaria dubia, 305, 319 S. concharum, 304
Rolandia coralloides, 129, 139, 143 S. vermicularis, 304, 316–318
Rossella nodastrella, 388 Sertularella gayi, 301
Ruvettus pretiosus, 310 Setosella
S. cavernicola, 309
S. vulnerata, 309
S Siboglinum sp., 304
Sabella pavonina, 304 Siphonidium ramosum, 300, 315
Sagartia Siphonodictyon infestum, 300, 313
S. elegans, 302, 315 Siriella sp., 307
S. troglodytes, 302, 315 Sladenia shaefersi, 342
Salmacina dysteri, 304 Smittina
Sarcodictyon catenatum, 129 S. cervicornis, 309, 323, 324
Sarritor frenatus, 344 S. crystallina, 309, 324
Saurida lessepsianus, 514 Smittoidea
Savalia savaglia, 127, 137, 138, 218, 427, 538 S. ophidiana, 309
Scalpellum scalpellum, 306, 320 S. reticulata, 309
Sceptrella insignis, 300, 313 Solatisonax bannocki, 305
Schizocyathus fissilis, 53, 85, 86, 89, 92, 132, 135, 149 Solenosmilia variabilis, 18, 398, 399, 407, 414, 415, 486,
Schizomavella 521, 524
S. cf. discoidea, 309 Sphaerosyllis cf. pirifera, 304
S. fischeri, 309 Sphenotrochus andrewianus, 127, 134, 136
S. linearis, 309 Sphyrna lewini, 341
S. neptuni, 309 Spinimuricea spp., 142
Schizoretepora longisetae, 309 S. atlantica, 129, 143
Schizotricha frutescens, 301 S. klavereni, 129, 143, 149, 453
Scleranthelia, 143 Spiochaetopterus sp., 304
S. rugosa, 129, 303, 315 Spiophanes sp., 304
S. rugosa var. musiva, 303 Spiroxya
Scolelepis sp., 304 S. heteroclita, 300, 313
Scorpaena spp., 325 S. levispira, 300, 313
S. elongata, 310, 325, 326 Spondylus gussonii, 296, 306, 316, 318
S. scrofa, 310, 325 Spongiobacter sp., 378, 382
Scrupocellaria Squalus blainville, 311
S. delilii, 309, 324 Stelligera rigida, 300
S. incurvata, 309, 322 Stenocyathus vermiformis, 16, 18, 19, 68, 70, 74, 75, 77,
Scyliorhinus sp., 338, 339, 349 78, 85, 86, 89, 91–93, 127, 132, 134–136, 302,
S. canicula, 311, 337–339, 341, 348–350 311, 315
S. retifer, 342, 345, 348, 349 Stephanocyathus, 52, 149, 150
S. stellaris, 338, 348 Stephanollona armata, 309, 323
Scyllarus arctus, 307, 321 Stephanophyllia sp., 74, 93
Scyphopodium ingolfi, 143 Stephanotheca
Sebastes sp., spp., 340–345, 350, 351 S. arrogata, 309, 324
S. aleutianus, 344, 349 S. watersi, 309
S. alutus, 343, 344, 348, 349 Stomatopora gingrina, 309
S. babcocki, 344, 349 Streptocaulus cf. pectiniferus, 301, 317
S. borealis, 344, 349 Stylocheiron suhmi, 307
S. ciliates, 344 Stylocordyla pellita, 300
S. ensifer, 344, 349 Stylophora pistillata, 395, 406, 525
S. fasciatus, 345, 349 Subadyte pellucida, 304, 318
S. jordani, 344, 349 Suberites sp. 1, 300
S. levis, 344, 349 Suberites sp. 2, 300
S. marinus, 340, 343, 348 Sudis hyalina, 310
S. mentella, 345, 349 Sulcastrella tenens, 300
S. polyspinis, 344, 349 Swiftia, 129, 142, 150
S. ruberrimus, 344, 349 S. pallida, 129, 140, 142, 162, 231, 246, 253, 303
S. rufus, 344, 349 S. rosea, 303
S. simulator, 344, 349 Sympagella delauzei, 301, 313, 314
S. viviparus, 340, 341, 344, 345, 348, 349 Synaphobranchus kaupii, 341
S. zacentrus, 344, 349 Synelmis sp., 304
554 Species Index
T V
Telestula septentrionalis, 129, 143, 149 Veretillum cynomorium, 130, 145–147, 234, 450
Tentorium semisuberites, 388 Vermiliopsis sp., 305
Terebratulina retusa, 309, 324, 325 V. monodiscus, 304
Tervia barrieri, 309 Vibilia armata, 306
Tessaradoma boreale, 309, 323, 324 Villogorgia bebrycoides, 129, 143, 231, 246,
Teuchopora edwardsi, 309 253, 338
Thalamophyllia gasti, 126, 132, 133, 302, 316 Viminella flagellum, 121, 128, 139, 141–143, 162, 213–215, 220,
Thrombus abyssi, 300, 313, 315 222–224, 229–231, 246, 303, 453
Timea chondrilloides, 300 Virgularia mirabilis, 130, 145–147, 235
Todarodes sagittatus, 306 Vulcanella gracilis, 300
Trachyscorpia cristulata, 342, 348
Tretodictyum cf. tubulosum, 301
Trisopterus minutus, 340, 348 Y
Trochocyathus sp., 74 Yoldiella lucida, 306
T. mediterraneus, 85, 86, 89, 91, 92, 132, 135
Tubiclavoides striatum, 301, 317
Turbicellepora coronopus, 309 Z
Turritopsis cf. nutricula, 301 Zaprora silenus, 344, 349
Zeus faber, 250, 338, 348
Zygophylax
U Z. biarmata, 301, 317
Upeneus moluccensis, 514 Z. cf. brownei, 301, 317
Subject Index
*When a keyword has more than 400 instances in the book, first instance page number from each chapter and page number where the term is
explained in detail are referred in the index.
A Age, 10, 15, 16, 20–22, 32, 48, 49, 53, 54, 58–60, 62, 67, 68, 70, 72,
AAMP, see Marine Protected Areas Agency 73, 76–80, 85, 86, 92, 95, 97, 98, 117, 157, 227, 267, 279, 296,
Abrupt salinity changes, 510 366, 384, 394, 399, 409, 413, 416–419, 425, 426, 428–430,
Abyssal, 122, 257 486–488, 517
plains, 3, 35, 249, 490 classes, 428–430
ACC, see Amorphous calcium carbonate Aggradations, 42, 57, 59, 60
Acclimation, 395, 417, 418, 439–441, 449, 450, 453, 464, 520, rates, 57, 59, 60, 62, 76, 111
522–526, 533 Aggregations, 77, 79, 158, 160, 163, 179, 214–220, 227–235, 237,
Accretion rate, 51, 54, 78, 80 250, 271, 277, 281, 287, 316, 322, 325, 343, 344, 363, 416, 535
ACES, 4, 475 Agriculture, 526
Aceste seamount, 219, 224 Ahermatypic, 73
Acidification, vii, 96, 396, 406, 417, 418, 437, 511, 531, 533, 536 Air bubbling, 448
Acoustics Air-sea exchanges, 200
backscatter, 157, 158, 176, 184 Air-sea fluxes, 198, 200
technologies, 173 Alaska, 343, 344, 348, 349, 473, 474
Acroporid corals, 382, 384 Albania, 218, 514, 538, 539
Acrylic, 443, 453 Alborán Ridge, 57, 220
Acrylic acid, 379 Alborán Sea, 5, 6, 17, 23, 32, 35, 41, 42, 57–64, 69, 76–78, 80, 99,
Actinians, 315 123, 124, 126–131, 135, 136, 138–140, 142–145, 147, 149,
Activated carbon, 443 157, 159–162, 174, 195, 216, 220–222, 226, 228–230, 234,
Adaptation, 9, 23, 144, 341, 357, 367, 377, 396, 399, 417, 459, 237, 247, 249, 261, 265–267, 273, 287, 298, 312, 313, 319,
460, 464 322–325, 327, 337, 338, 363, 515, 542
ADELIE, 177, 178 Alcyonacea, 6, 121, 122, 127, 138–143, 149, 229–231, 427, 541
Adenosine triphosphate (ATP), 395 Alcyonaceans, 127, 139–142, 149, 180, 214, 216, 220, 229–233, 237,
Adriatic Deep Water (ADW), 164, 199, 207, 235, 236, 286, 364 253, 254, 347, 486, 488, 538, 540
Adriatic Sea, 24, 42, 98, 100, 131, 135, 138, 173–176, 199, 202, Aleutian Islands, 344, 345, 349
216–218, 225, 228, 230, 234–236, 261, 262, 272, 286, 297, Algae, 90, 91, 122, 377, 427, 444, 456, 466, 467, 537
311, 313, 319, 320, 324, 347, 364, 365, 418, 500, 502, 507, Algerian basin, 207
515, 542 Algerian coast, 207
Adult, 133–135, 219, 259, 298, 325, 337, 341, 343, 350, 419, 424, Algerian Eddies, 207, 490
430, 453, 456, 461, 484, 489, 491, 493, 495, 513, 533 Algerian margin, 236
Aegaeo research vessel, 257 Algero-Provençal basin, 236, 501
Aegean Deep Water, 235, 364–365 Alizarin red, 412
Aegean Sea, 5, 32, 85–93, 131, 135, 138, 147, 197, 199, 225, 226, Alkalinity anomaly, 394, 411, 455
228, 230, 249, 279, 324, 365, 418, 500–503, 507, 515 Almeria-Oran front, 491
Aeration system, 438 Along-path trajectories, 493
Aerobic, 395 Along-slope contourite deposits, 35, 36
Aesthetic, 475 α-diversity, 221
African humid period, 266, 267 Alphaproteobacteria, 380, 381, 383
African plate, 499–501, 503 Amanthea Basin, 48
Agassiz trawling, 278–280 Ambient bottom seawater, 438, 441

https://doi.org/10.1007/978-3-319-91608-8
556 Subject Index
Amino acids, 378, 383, 392, 395, 453, 459 Architectonicidae, 22

Ammonium excretion, 440 Architects, 16, 475
Amorphous calcium carbonate (ACC), 405, 406, 409 Architecture, 109, 336, 360, 361
Amphipods, 319 Archive, 5, 23, 42, 67, 95–97, 104, 358, 374, 406, 455, 510
tubes, 336 Arctic Sea Ice Forum, 474
Anaerobic oxidation, 262 Areas beyond the limits of national jurisdiction (ABNJ), 537
Anastomose, 136 Argille Azzurre Formation, 75
Anastomosis, 318 Argocrete, 454
Anatomy, 122–123, 125, 131, 137–139, 148, 406, 407 Argo Program, 204
Anaximenes ridge summit, 196 ARISA OTUs, 379–381, 383
Ancient literature, 67, 74 Artificial
Angola, 440 food, 395
Angola margin, 342 sponge, 454
Animal forest, 213, 231, 237, 249, 250, 316, 427, 473 substrate, 430
Anisotropic, 426 Artificial seawater (ASW), 439, 448
Annual bands, 409, 410 Artisanal fisheries, 214, 215, 250, 251
Annually-banded aragonite, 99 Asexual/asexually, 358, 359, 416, 454
Annual patterns, 409 Asexual reproduction, 132, 358, 359, 398, 485
Annulus kernel, 162 Assemblage, 5, 6, 19, 21, 22, 31, 32, 48, 54, 61, 73, 74, 80, 125, 138,
Anomurans, 320 158, 159, 180, 182, 191, 194, 209, 214, 217, 219, 220, 226,
Anoxia, 458, 508–509 227, 237, 245–247, 250, 253–254, 259, 296, 298, 311–313,
Anoxic, 52, 165, 261 318–320, 322, 325, 327, 341, 342, 501, 515, 539, 542
Anoxic bottom water conditions, 98 Assimilated carbon, 459
Anthoathecata, 6, 121, 122, 130, 148, 541 Assimilated model, 495
Anthozoa, 122–131, 138–147, 214, 227, 228, 231, 233, 247, 249, 253, Assimilated nitrogen, 459
254, 259, 301, 302, 304, 315–316, 327, 450, 475, 538, 539 Assimilation products, 197
Anthropogenical, 96, 509, 517 Associated fauna, 7, 8, 10, 11, 20, 76, 194, 219, 245, 253, 254, 258,
Anticyclonic Cyprus Eddy, 200 276–278, 280, 281, 295–328, 340, 349, 367, 377, 406, 535
Anticyclonic eddy(ies), 200–202, 490 Associated species, 7, 8, 75, 77, 159, 221, 258, 263, 281, 297, 312,
Antifouling, 298, 407 320, 322, 327, 367, 531, 535, 539
Antipatharia, viii, 6, 121–126, 131, 137, 149, 163–167, 180, 213, 214, Asteroid, 320, 322
219, 227–229, 236, 237, 249, 251, 253, 261–263, 315, 320, Aswan High Dam, 491
338, 340, 348, 388, 412, 413, 439, 453, 460, 513, 515, 535, Atlantic
538, 540, 541 affinity, 41, 115
Apennines, 74, 75 banks, 312
chain, 16 basin, 61, 249
Aphotic benthos, 490 counterparts, 116, 296, 312
Apulian Adriatic, 236 Atlantic Meridional Overturning Circulation (AMOC), 510
Apulian margin, 76, 92, 218, 237 Atlantic Ocean, vii, 6, 8, 21, 35, 36, 39, 42, 47, 51, 61, 77,
Apulian Plateau, 163, 236, 380, 382, 383, 387, 388 115, 116, 173, 174, 178, 182, 213, 221, 222, 229, 231,
Apulian Platform, 379, 381, 382 298, 312, 318, 322, 360, 363–365, 417, 439, 491, 499,
Aquaculture, 255, 448, 468, 513, 542 501, 502, 507, 510
Aquaria, 9, 10, 100, 361, 374, 395, 405–408, 411, 412, 414–418, 429, Atlantic rocky shores, 428
435–468, 474, 488, 531, 532 Atlantic Water (AW), 130, 197–201, 209, 266, 365, 396, 489,
infrastructure, 436, 437, 442, 445, 446 507, 508
Aquaria-based, 437 inflow, 36, 201, 206, 508
Aquarium, 437–440, 442, 443, 445, 448–450, 452, 453, 464–468, 474, Atlanto-Mediterranean
519, 531 distribution, 10, 315, 322
Arabia, 500, 501, 503 species, 79, 227, 229, 230
Arabia-Eurasia collision, 501 ATLAS, vii, x, 11, 328, 339, 369, 467, 475, 476, 479
Aragonite Atmosphere, 98, 503, 518
allochems, 17 Atmospheric forcings, 197, 281
dissolution, 17, 74 Aturia Layer, 74
gravel, 449 Australia, 373, 541
saturation state, 99, 103, 235, 519, 522, 523 Australian region, 489
Aragonite saturation horizon (ASH), 518 Authigenic
Aragonitic, 17, 19, 122, 518 carbonates, 261, 267
Aragonitic skeletons, 15, 41 limestones, 117
Arborescent, 133, 135, 227, 228, 230, 249, 250, 286–287, 338, 540 Authorities, 165, 254, 257, 259, 439
Archaea, 8, 378, 387–389 Autofluorescence, 388
Archaeal community, 387 Automated classifications, 6, 157, 162, 163
Archaeal primers, 387 techniques, 159
Archaeon, 388 Automated Ribosomal Intergenic Spacer Analysis (ARISA),
Archeobacteria, 262 379–381, 383
Archi, 18 Automatic classification, 160, 162–163, 165–167, 178, 181, 182, 184
Archimedes’ Principle, 411 Autonomous benthic landers, 338, 340
Subject Index 557
Autonomous underwater vehicles (AUVs), 158, 159, 177, 178, 184 Behavior, 147, 191, 322, 341, 392, 399, 426, 430, 453, 484, 486–488,
Avempace bank, 222, 321, 322 492, 493, 495
Awareness, 477, 478, 518, 535 Behavioural pattern, 337
Axis, 122, 124, 125, 137–139, 141–143, 258, 275, 276, 279, 285, 399, Belgica Mound Province, 22–23, 340, 341
410, 412, 451, 453, 454, 494, 522, 523 Belsito, 74
Azooxanthellate, 71, 74, 75, 79, 99, 101, 122, 132, 148, 214, 373, 374, Benthic biodiversity, 31, 285, 317
393, 407, 436, 535 Benthic biota, 16, 53
Azores, vii, 341, 348, 361, 362, 413, 438, 445–447, 453, 454, 468 Benthic Ecogeochemistry Laboratory (LECOB), 444, 468
Benthic epifaunal, 177
Benthic foraminifer record, 23
B Benthic lander, 337, 338, 340
Backscatter, 160, 162, 164, 168, 176, 178–182, 184, 185, 267 Benthic pelagic coupling, 245, 313
Bacteria, 261, 377–379, 382–384, 387, 388, 443, 452, 459, 460, Benthic Positioning Index, 162
467, 489 Benthic production, 396
Bacterial community composition (BCC), 377–379 Benthic system, 245
Bacterial growth, 396, 449, 461 Benthic Terrain Modeller, 162, 175, 274
Bacterial host, 415 Benthopelagic, 318, 337, 350
Bacterial production, 378 Benthoscape, 179, 182
Bacterial productivity, 262 Berna Convention, 251
Baffling effect, 40, 61 Betic corridor, 47, 48
Baited cameras, 338, 340, 341 Beverton–Holt model, 424
Balanid(s), 319, 320 Bicarbonate, 100
assemblages, 320 ions, 518
Baldissero Formation, 73–74 Bioclastic debris, 161
Balearic Basin, 279 Bioclasts, 111, 161
Balearic Promontory, 320, 325 Biocoenose des “coraux blancs”, 32, 85, 296
Balearic Sea, 21, 98, 222, 234, 338, 339, 347 Biocoenosis, 22, 32, 227, 258, 296, 313, 315, 322
Balkan, 235 Bioconstructions, 16, 19, 52, 53, 67, 68, 71, 75, 79, 80, 161, 165, 176,
Bamboo coral, 161, 232, 233, 246, 247, 298, 339, 427, 475–477, 536, 213, 214, 216, 221, 315, 324
538, 539, 542 Biodiversity, vii, viii, 10, 11, 31, 32, 121–151, 159, 165, 191, 192,
Banc de Provençaux, 62 237, 253, 259, 262, 271, 281, 293, 295, 296, 298, 311, 312,
Band intensity, 379 317, 320, 324, 327, 350, 368, 377, 405, 406, 419, 431, 462,
Band variability, 383, 384 467, 473, 475, 507, 508, 511, 513, 519, 533, 535–537, 539,
Banyuls, 32 540, 543
Barcans, 42 hotspot, 7, 8, 15, 253, 261, 263, 298, 313
Barcelona Convention, 138, 160, 251, 259, 439, 476, 537–539, 542 Bio-ecological, 60
Bari, 216, 286, 287, 339 Bioenergetics approach, 413
Canyon, 23, 32, 37, 42, 116, 174–179, 181–183, 185, Bioeroded, 16, 76
216–218, 225, 226, 236, 272, 286, 295, 297, 311, 313, Bioeroding organisms, 452
315, 317, 323 Bioerosion, 17, 18, 313, 417
Barnacles, 16, 19, 219, 320 paths, 24
Baroclinic, 202, 274, 490 Biofilm, 17, 454, 467
flow, 197 Bio-filter, 411, 443
Barotropic, 197, 207 Bioformation, 427
Barriers, 203, 360, 373, 491 Biofouling, 17
Basal deposits, 19 Biogenic
Basal portions, 258, 313, 315 carbonates, 39, 101, 318, 411, 455
Basaltic slabs, 161 frames, 298
Basinal decline, 117 habitats, 341
Basin-scale, 51, 53, 67, 79, 168, 213, 318, 502 interstices, 298
Bathyal origin, 161
biocoenoses, 52 Biogeochemical, 462, 518
corals, 5, 47, 85–93, 135 Biogeochemical cycling, 398
depths, 15, 19, 42, 48, 85, 131, 149, 227, 315 Biogeographic dispersion, 398
habitat, 53–54, 325 Biogeographic traits, 214
muddy bottoms, 232, 319, 320 Biogeographic variability, 396
setting, 15, 19 Biogeography, vii, viii, 4, 6, 8, 25, 115, 141, 213–238, 377, 490
Bathymetric distribution, 135, 192–194, 213, 229, 230, 233, 234, 245, Bioherms, 265, 340–342
246, 249, 271, 324 Bio-limiting macronutrients, 103
Bathymetric Position Index (BPI), 158, 175, 176 Biological clocks, 410
Bathymetric range, 6, 135, 137, 138, 147, 149, 216–217, 226, 227, Biological connectivity, 483–495
229–231, 235, 312, 317, 427, 428, 430, 513, 514 Biological diversity, 164, 537–539
Bay of Biscay, 144, 149, 341, 348, 359, 361, 362, 489 Biological filter, 349, 439
Bedrock Biological filtration, 443, 447
cliffs, 93 Biological overprint, 98, 104
overhangs, 285, 297, 490 Biological pump, 103
558 Subject Index
Biology, vii, 4, 7, 104, 233, 237, 361, 363, 391–399, 406, 419, 437, Branches
448–449, 452, 467, 475, 487, 489, 492, 510, 519 canyon, 291
Bioluminescent, 316 coral, 292, 293, 298, 313, 320, 339, 341, 347, 408, 412, 416,
Biomass, 10, 263, 272, 276, 278, 279, 311, 313, 320, 337, 340, 349, 454, 467
377, 413, 473 Branching
Biomineralization, 5, 95, 96, 103, 104, 406, 411, 416, 455, 462, form, 393
464, 526 scleractinians, 16
Biophysical model(ing), 195, 430, 483–495 typology, 75
Biosphere, 6, 215, 271, 499 Brèche Rouge, 48, 74, 75
Biotin carboxylase, 388 Breeding, 335, 337, 345, 351, 452
Bioturbation, 36, 111, 158, 192 habitat, 325, 335, 384
Biozone MNN19f, 76 Bremen Seafloor Drill Rig, 62, 76
Bitlis, 503 Brines, 261, 452, 525, 526
Bitlis suture zone, 500, 503 British Columbia, 344, 349, 351
Bivalves, 18, 19, 21, 76, 110, 162, 261, 292, 296, 312, 314, 318, Brittle star, 140, 320
408, 467 Brittlestar Ridge (BR), 58, 62, 63
Black corals, 6, 124, 125, 131, 137, 138, 159–161, 166–167, 214, Broadcast, 398, 399, 461, 485–490
227–229, 245–247, 249–251, 253, 311, 315, 316, 322, 325, spawners, 398, 399, 461, 485–490
326, 335, 337, 338, 344, 348, 349, 427, 447, 450, 451, 453, Brooded larvae, 486, 487
454, 536, 538–542 Brooding, 398, 485–488, 494
Black Sea Bryozoans, 17, 19, 23, 25, 53, 62, 75, 76, 79, 111, 162, 258, 259, 292,
rivers, 509 295, 297, 312, 322–324, 327, 473, 539
Water, 198 Budding, 135, 136, 394, 467
Blanes Canyon, 7, 271, 274, 276, 278–280, 286, 287 rate, 393, 411, 413, 415, 455
Blastulae, 488 Building-up mounds, 57, 60
Bleaching event, 382 Build-ups, 52, 58, 62, 79, 158, 217, 221, 261, 267, 440, 443, 452, 460
Blogs, 474 Bulk density, 110
Blue biotechnology, 542 Buoyancy, 430, 484, 488, 492
Blue energy, 542 loss, 198, 199
Blue Growth, 542 Buoyant, 365, 461, 488, 490, 492
Blue shrimp, 320 weight, 394, 411–412, 415, 454, 455
Bølling-Allerød (BA), 54, 58, 59, 67, 77–79, Burdigalian-Langhian, 48, 49
265, 266 Burial, 32, 42, 176, 221, 235, 262, 266, 417, 465, 508
Bonn Convention, 160 Burial alteration, 17
Book shelf faulting, 503 Burrowing habits, 327
Boreal fauna, 315 Bushes, 125, 133, 135, 142, 221, 286, 359–360
Boring(s) Bycatch, 116, 215, 226, 232, 234, 237, 249, 250, 296, 346, 347, 359,
sponges, 313 437, 519, 536, 540
traces, 19
Boron isotopes pH proxy, 95, 101
Boron isotopic composition, 101–103 C
Bosphorus, 501, 503 Ca-ATPase pump, 102
Bottle-brush, 125, 228, 250 Cabliers banks, 58, 59, 130, 136, 138, 161, 297, 298, 303, 311, 314,
Bottom contact gears, 536 321, 322, 325, 326
Bottom currents, 5, 19, 20, 23, 35–42, 62, 63, 158, 162, 163, 175, 234, Cabliers Mounds, 62, 161
258, 261–263, 281, 342, 350, 384 Cabo de Gata, 32
Bottom-current velocity, 37, 262 Cainozoic, 68, 115
Bottom fishing gear, 250, 347 Calabria, 18–20, 48, 74, 115, 238, 250, 251
Bottom trawl, 30, 341, 345 Calabrian Arc, 265, 500–502
Bottom trawling, 10, 159, 214, 245, 247, 250, 293, 312, 346, 475–477, Calabrian stage, 52, 53, 67, 76, 79
538, 541 Calabria-Sicilian margin, 236
Bottom trawl nets, 165 Calcare di Mendicino, 48, 74
Bottom-up approaches, 158, 159, 174, 182–184 Calcarenites, 75
Boulders, 18, 19, 22, 52, 71, 76, 160, 165, 166, 217, 274, 292, 311, Calcareous framework, 221, 313
315, 336, 340, 346 Calcareous plankton, 48
Boundary, 48, 51, 54, 67, 78, 79, 413, 500, 501, 503 Calcein, 412
Bourcart, 193 Calcification, 10, 103, 377, 391–395, 399, 405–409, 411, 412,
Canyon, 192, 286, 287, 338 416–418, 441, 442, 455, 458, 460, 462, 464, 466, 517,
Box core, 69, 377–379, 437, 441 520–525, 531–533
Box-corer, 22, 62, 177, 184, 441 rate, 10, 384, 393–395, 397, 411, 415, 417, 418, 440–442, 455,
Box-coring, 21, 25, 76, 79 462–464, 520, 522, 531–533
Brachiopods, 16–18, 22, 75–76, 295, 324–325, 327 Calcifying, 99, 102, 103, 405–419, 455, 526
Brachycnemic, 137 organisms, 22, 405, 406, 418, 518
Brackish Calcite, 23, 139, 405, 518
Lago Mare, 48, 49 Calcitic
solution, 453 octocorals, 16
water, 48 skeletons, 17
Subject Index 559
Calcium carbonate Cassidaigne canyon, 32, 137, 183, 185, 192–194, 196, 207, 272, 286,
compounds, 405 287, 291, 311, 313, 315, 336, 338, 347
saturation state, 518 Catalan-Provençal-Ligurian canyon, 32, 41, 195, 219, 298, 312, 315, 322
Calibrated ages, 70, 98 Catalan-Provençal margin, 515
Calibration, 47, 68, 100, 101, 103, 104, 409, 410, 416 Catalonia, 75, 147, 222
equations, 95 Catalysed Reporter Deposition–Fluorescence In Situ Hybridization
Calices, 22, 374, 407 (CARD-FISH), 388
Calicoblastic, 409, 524 Catania, 18, 54, 80, 323
Calicular structures, 123, 135 Catifas Bank, 136, 314, 322, 326
Calypso, 32 Cauliflower-like pattern, 176
Camaro, 19 Caves, 126, 127, 219, 292, 324, 539
Camouflage, 320, 338 Cellular debris, 460
Canada, vii, 342, 349, 412, 473, 474 Cellular respiration, 395
Canary Islands, 341 Cellular stress response, 464
Candelabrum-shaped, 232 Census, 423, 424, 542
Cannes Canyon, 192, 234 Centennial, 96, 104
Canopy, 21, 22, 227, 250 Centers of calcification (COC), 97, 100, 408, 409
Canyon Centers of rapid accretion (CRA), 97, 409
floor, 274 Central Mediterranean, vii, 5, 6, 10, 31, 32, 95, 96, 159, 235, 295, 297,
head, 191, 221, 272, 274, 285–287, 291, 292, 415, 444 315, 318, 319, 324, 337, 339, 367, 414, 501, 502
Cap de Begur, 291–293 Centre Scientifique de Monaco (CSM), 439, 444–445, 455–457, 468
Cap de Creus, 219, 274, 275, 428 Centuries, vii, 3, 4, 17, 31, 32, 73, 97, 115, 116, 121, 125, 131, 135,
Cap de Creus canyon, 4, 7, 11, 32, 207, 219, 271, 272, 274, 276, 141, 145, 148, 149, 196, 208, 221, 226, 232, 249, 271, 340,
278–280, 286, 287, 291, 297, 298, 324, 325, 347, 411–413, 351, 391, 395, 417, 418, 428, 429, 437, 473, 503, 507,
416, 418 509–511, 515, 517–520
Cape Lookout, 345 Ceriantharians, 327, 513, 515
Cape Tres Forcas, 221 Cerianthids anemones, 336
Capo Milazzo, 18, 19, 70 Challenger Mound, 17, 22
Capo Spartivento, 219, 297, 311, 324 Chambers, 397, 411, 440–442, 445, 451, 452, 454, 456–458, 460,
Carbon 461, 465
isotopes, 96, 99, 100, 393 Changes in pressure, 437
isotopic signature, 392 Changing Oceans Group, 447, 462
sequestration, 237, 405 Cheilostomes, 322–324
stores, 460 Chella Bank, 6, 57, 130, 131, 136, 138–140, 145, 157, 159–163, 166,
Carbonate 168, 222, 297, 298, 311, 313, 321, 322, 325, 326, 539
chemistry, 96, 103, 395, 440, 442, 447, 449, 518, 533 Chemical agents, 466
chimneys, 317 Chemical dispersant, 465
compensation, 536 Chemical equilibrium, 466–467
crystal formation, 406 Chemical filter, 439, 461
ions, 103, 104, 518 Chemical filtration, 438, 443, 449
lattice, 101 Chemical markers, 412
skeletons, 406 Chemical properties, 158, 167, 440
structure, 68, 393, 412 Chemical receptors, 439
surfaces, 19 Chemoautotrophic activity, 460
system, 96, 204, 463, 464 Chemoautotrophy, 393
Carbonate-dominated Facies (CF), 75 Chemosynthesis, 261
Carbon balance, 536 Chemosynthesis-based communities, 261
Carbon cycling, 10, 349 Chemosynthetic, 261, 262
Carbon dioxide (CO2), 103, 391, 405, 406, 417, 440, 447, 448, 458, Chilean fjords, 97, 103, 487
462–464, 517–520, 531 Chilean Patagonian fjords, 486
budget, 405 Chiller, 438–441, 444, 445, 448–450
Carboneras, 48, 74, 75, 150 Chimneys, 261, 262, 317
Carbonic acid, 406, 518 Chitin, 249
Carbonic anhydrase, 406, 418, 521, 522 Chlorophyll, 160, 197
Caribbean, 10, 412, 513 Chronological calibration, 410, 416
corals, 388 Chronostratigraphic, 67, 79
Carloforte shoal, 232, 250 Cilia, 488
Carnivorous, 513, 515 Ciliary, 461, 465
sponge, 193, 313 Ciliated planula, 487
Carotenoids, 452, 461 Circalittoral
Carrying capacity, 351, 424 environments, 18, 52, 73, 75
Cartilagineous, 325 habitat, 53, 325, 341
Cartilaginous fishes, 347–349 Circuit, 200, 438
Cartridge filters, 450, 452 Circulation
Cascade, 195, 199, 207, 235, 237, 285, 286, 415, 418, 490 patterns, vii, 8, 207, 266, 383, 490
Cascading dense water plumes, 199 properties, 8, 195
Cascading effect, 213, 237 Cirripedia, 306, 320
560 Subject Index
Cirripeds, 19 biocoenosis, 296, 313, 322

CITES, 251, 439 bioconstructions, 16, 52, 68, 79, 80, 176, 214, 216, 221, 324
Classes, 122–148, 160, 162–164, 166, 167, 180, 185, 194, 277, 280, carbonate factory, 16
383, 388, 425, 428, 429 frame builders, 16
Clayey matrix, 267 geochemistry, 23, 41, 96, 99, 104
Clayey sediment, 19 habitat, vii, 3, 7–9, 16, 17, 19, 22, 23, 39, 78, 163–165, 167, 168,
Clay matrix, 18 173–186, 195–209, 214–216, 291–293, 295–327, 335–351,
Cleavage, 398 358, 367, 417, 437, 439, 499, 502, 507, 508, 510, 511, 518,
Cliffs, 21, 22, 93, 131, 184, 193, 265, 286, 427 525, 539, 540
Climate living grounds, 507
change, 11, 51, 95, 208, 378, 391, 392, 395, 398, 399, 405, 417, plastering hard substrates, 18–20
418, 428, 430, 431, 436, 437, 440, 447, 454, 474, 499, 503, province, 6, 22, 32, 33, 37, 40–42, 62, 64, 157, 159, 163–168, 178,
507–509, 513, 515, 517–521, 525, 526, 535–537, 542 207–209, 215–229, 232, 234–237, 253, 273, 286, 295–297,
degradation, 41 313, 319, 324, 337, 338, 346, 347, 351
events, 517 reef resilience, 406
fluctuations, 51–54 Cold winds, 235, 507
forcing, 51 Collina di Torino, 73
history, 96 Colonial, 16, 18, 19, 48, 68, 71, 74–77, 79, 80, 85, 86, 121, 123, 124,
model, 507, 509–511, 536 130–138, 147, 149, 214, 221, 228, 233, 249, 261, 263, 314,
oscillations, 52–54 324, 336, 345, 363, 374, 398, 407, 410, 411, 413, 415, 450,
perturbations, 507–508 455, 458
system, 507, 510, 511, 517 growth, 485
transient events, 510 Colonisation, 22, 23, 39, 41, 42, 48, 59, 165, 213, 261, 262, 357, 358,
trends, 96 363, 365, 368, 384, 398, 405, 417, 426
Climatic forcings, 42, 47 Commensal polychaete, 19, 22
Climatic hot-spots regions, 197 Commercial fisheries, 31, 335, 346, 351
Climatic records, 97 Commercial interest, 8, 9, 11, 150, 285, 320, 346
Climatological, 60 Commercial species, 214, 250, 311–312, 344, 351, 539
Clonality, 357–360 Commercial trawling, 159, 274, 292
Clonal propagation, 426 Communities∗, 3, 17, 31, 47, 51–54, 57, 62, 74, 85, 101, 121, 157,
Clone libraries, 379, 380, 382, 384, 388 173, 194, 196, 213, 245, 249–251, 254, 257, 261, 267, 272,
Closed system incubations, 442 285, 291, 295, 335, 360, 374, 377, 387, 391, 406, 444, 473,
Closed water circulation systems, 437 511, 513, 531, 536
Closure areas, 540, 541 COMP, 384, 441
Clumped isotope(s), 100 Compartment, 123, 327, 406, 413, 440
vital effects, 100 Competition, 410, 416
Cluster analysis, 378 Complex image analysis algorithms, 158
Clusters, 42, 58, 61, 62, 77, 78, 159, 181, 182, 217, 219, 221, 276, Complexity, 157, 158, 167, 197, 257, 262, 267, 272, 298, 311, 312,
277, 286, 292, 297, 361, 362, 378, 379, 382, 408, 409 318, 335, 336, 342, 346, 410, 411, 416, 436, 473, 484, 485,
CMECS, 185 495, 533
Cnidae, 123, 137, 452 Compressive settings, 261
Cnidaria, 6, 8, 52, 121–124, 160, 301, 302, 538 Computed-tomography (CT), 9, 24, 109–112
Cnidarian-predatory, 22, 319 Computer modeling, 483, 491
Cnidarians, 15, 16, 79, 122–124, 131, 139, 147, 150, 173, 185, 213, Conference of Parties, 538
214, 253, 261, 295, 312, 314–320, 322, 324, 327, 347, 406, Congener, 142, 325, 395, 399, 493
484, 510 Conglomerate layer, 18
Cnidocyst, 460, 487 Connectivity, 8–9, 195, 217, 357–369, 373, 398, 426, 430, 431,
Cnidom, 373 483–486, 488–495, 499, 501, 502, 542
Coarse grained deposits, 92 Conservation, vii, 7, 9–10, 138, 150, 159–161, 164–165, 173, 194,
Coarse sands, 90, 136, 161–163, 292 232, 247, 249, 253, 254, 257, 259, 263, 281, 298, 328, 347,
Coarse sediments, 85, 418 351, 357, 360, 365, 367, 368, 399, 405, 419, 423–431,
Coastal tourism, 542 473–475, 478, 483, 514, 535–543
Cobbles, 336 Conspecific, 10, 359, 457
CoCoNet, 25, 42, 80, 105, 112, 117, 178–183, 186, 238, 328, 360, Contamination, 103, 379, 388, 438, 441
365, 369, 375, 467 Continental collision, 499–501, 503
Coelenterons, 123, 378 Continental margin, 10, 36, 57, 61, 76, 181, 183, 219, 221, 247, 272,
Coenosarcs (CS), 298, 406, 407, 521 274, 275, 285, 298, 316, 340, 349, 361, 383, 392, 413, 501, 502
Cohort, 398, 429, 484, 487, 489 Continental shelf, 3, 4, 6, 35, 158, 191, 219, 227, 234, 245–247, 249,
Cold rooms, 438 250, 257, 274, 280, 287, 340, 344, 363, 427, 453, 513, 514
Cold-seep communities, 267 Contour currents, 35, 41
Cold-water carbonate bioconstructions, 161 Contourites, 5, 35–42, 262
Cold-water coral (CWC) deposits, 35–39, 262
banks, 216, 221, 229, 234, 312–315, 317–319, drifts, 5, 35–38, 41, 42
322, 327 facies, 36, 39, 41
bearing cores, 23, 109–112 moats, 42
bearing deposits, 18, 48 Controlled experiments, 437
Subject Index 561
Controlling factor, 267, 489 Crest, 58, 62, 161

Convention on Biological Diversity (CBD), 537 Cretaceous, 68
Conveyor belt, 39 Cretan arc, 235
Cool boxes, 439 Cretan Intermediate Water (CIW), 197, 199
Cooling event, 54 Cretan Passage, 201
Cooling system, 445 Crete, vii, 17, 23, 36, 70, 77, 85, 87–93, 201, 202, 225, 265, 297,
Cool-rooms, 438, 444 503, 515
Copepods, 319, 451, 452, 456, 461, 467 Crinoids, 53, 262, 314, 321, 322
Copernicus Marine Environment Monitoring Service (CMEMS), 202, Critical habitats, 8, 335–351, 514–515
203, 207–209 Critically endangered, 141, 214, 232, 247, 476, 538
Coral associated bacterial communities, 444 Croix St. André, 441, 442
Coral-bearing sediment cores, 95, 104 Crossed-lamellar, 405
Coral bioconstructions, 16, 213, 324 Crude oil, 465
Coral bioeroder, 317 Cruises, vii, 31, 32, 54, 62, 69, 70, 96, 112, 151, 160, 191–194, 196,
Coral bush, 221, 359 200–202, 204, 205, 226, 257–259, 281, 360, 361, 367, 369,
Coral calcification, 100, 317, 318, 407, 416 436, 440–442, 464, 476, 515
Coral calcifying fluid, 99, 102, 526 Cruise tourism, 542
Coral canopy, 22, 250 Crustaceans, 3, 147, 253, 271, 277, 295, 311, 319–320, 325, 327, 340,
Coral Cemetery, 117 350, 467, 539
Coral coverage, 176, 342 Crusts, 164–166, 261, 262, 320, 321
Coral-cryptic behavior, 341 Cryos, 32
Coral deposits, 51, 86, 93 Cryptic organisms, 317
Coral fauna, 20, 51, 54, 74, 79, 121, 123, 148–150, 227 Cryptic species, 129, 137
CoralFish, 4, 168, 238, 343, 351, 360, 369, 475 Crystal, 406, 408–410, 416, 427
Coral framework, 32, 40, 57, 71, 121, 135, 149, 164–167, 216, Crystalline phases, 103
219–221, 229, 262, 314, 315, 319, 326, 337, 339–342, 345, CSM, see Centre Scientifique de Monaco
363, 416 CSNet mooring, 196
Coral garden, viii, 6, 159, 160, 162, 163, 245–247, 338, 359, 427, CTD casts, 157, 159, 160, 162, 164
541, 542 CTD profiles, 490
Coral geochemistry, 96, 104, 105 Ctenostomes, 322–324
Coral grounds, 22, 217, 296, 314 Cultivate, 436
Coralligenous, 158, 322 Cup coral, 161, 344, 410, 517
deposits, 92 Current speed, 195, 281, 350, 418, 439, 444, 456
Coralliophilinae, 319, 327 Cyana manned submersible, 20
Corallite, 69, 70, 74, 133, 394, 408–410, 524 Cyanobacteria, 467
Corallivorous gastropods, 21, 22 CYCLAMEN, 257–259, 399, 467, 474
Corallofauna, 18, 19 Cyclonic circulation, 201, 207, 507
Coral microhabitats, 387 Cyclonic eddies, 490
Coral microstructures, 97, 100 Cyclonic gyre, 199–201
Coral mound, 5, 16, 35, 40–42, 51, 54, 57–64, 73, 76–79, 111, 167, Cyclops, 416, 451, 453
176, 184, 215, 234, 262, 337, 338, 340, 342, 346, 508 Cyclostomes, 322–324
accretions, 51, 54, 76, 78 Cylindrical aquaria, 456
Coral patches, 97, 267, 293 Cyprus, 7, 32, 135, 202, 206, 225, 226, 257–259, 297, 322, 396, 466,
Coral probiotic hypothesis, 376 468, 485, 515, 536
Coral propagules, 8, 39 Cyprus Basin Oceanography (CYBO), 204
Coral proxies, 95, 104 Cyprus Eddy, 200, 204, 490
Coral ramifications, 315, 338
Coral rubble, 19, 57, 69, 92, 158, 160, 161, 166, 167, 265, 287, 298,
311, 315–322, 325, 326, 339, 340, 346, 417 D
Corals baffling sediment, 19 Damage, 4, 150, 162, 214, 247, 285, 291, 293, 344, 346, 347, 351,
Coral sea, 117 437, 438, 443, 473, 485, 513, 536
Corals three-dimensional structures, 135, 341, 406, 473, 531, 533 Dardanelles inflow, 509
Coral viability, 437–439 Dardanelles Straits, 508
Cores, 9, 22–24, 40–42, 58, 59, 62, 76, 78, 79, 95, 104, 109–112, 139, Dark, 31, 196, 249, 254, 266, 377, 391, 393, 395, 398, 410, 427, 438,
163–165, 167, 192, 200–202, 204, 207, 219, 254, 266, 361, 444, 445, 461
507, 509, 542 Dark Habitats Action Plan, 539
microbiome, 377–379, 383 Data assimilation, 197
Coring, 21–23, 76, 79, 267 Database, 67, 68, 80, 92, 103, 184, 192, 287, 540
CorSeaCan cruise, 191–194 Dating, 10, 20–23, 31, 41, 42, 54, 59, 76, 78–80, 95, 97, 98, 111, 112,
Corsica, 143, 191, 193, 207, 230, 236, 300, 500, 501, 536 117, 141, 227, 296, 360, 367, 411, 413, 414, 455
Corsica Channel, 42, 207, 236 Dead branches, 313, 315
Cosmopolitan, 53, 147, 234, 272, 322, 357, 378, 487 Dead Sea Fault (DSF), 500
Coupled climate models, 509, 510 Debris, 18, 19, 86, 93, 161, 265, 340, 346, 347, 460, 514, 535
Courtship, 335, 345 Decadal connectivity, 484
Crab, 250, 292, 319, 320, 384, 514 Decadal fluctuation, 204
Crenarchaeota, 387, 388 Decapods, 277, 280, 306, 319–321, 327, 340, 467
562 Subject Index
Decline phase, 51, 76, 80 Dhaka mud volcano, 266, 267

Deep basins, 47 Dohrn canyon, 21, 297, 312
Deep-coastal bottoms, 245–247 Diachronous, 54
Deep convection, 202 Diagenetic
Deep-corals, 32, 215, 232, 237, 245, 246, 298, 345, 423–431, 536 alterations, 23
Deep flow, 197, 490 processes, 17, 19, 20, 25, 111, 112
Deep-infaunal foraminiferan, 76 Diapir, 7, 57, 261, 265, 266
Deep layer, 8, 96, 196, 198, 495, 507, 510 DIC, see Dissolved inorganic carbon
Deep ocean, 391, 399, 447, 479, 492, 495, 518 Diel cycles, 488
Deep-sea benthic biota, 52–53 Diel migrations, 493
Deep-sea benthopelagic fauna, 337 Diffusion, 492–494
Deep-sea biota, 16 Digital Elevation Model (DEM), 175, 177
Deep-sea fisheries, 9, 475, 535, 538, 540 Digital holographic microscopy (DHM), 397
Deep seafloor, 52, 74, 346, 476 Digital terrain models (DTM), 158, 166
DeepSeaLab Instituto do Mar, 445–447 Dimethylsulfonioproprionate (DMSP), 379, 521
Deep-sea molluscs, 318, 488 DIP, see Dissolve inorganic phosphorous
Deep-sea mussels, 379 Disease, 378, 485, 489
Deep sea realm, 9, 25, 257, 259 Dispersal
Deep-sea shrimp, 509 distance, 359, 485–488
Deep-sea sponges, 440 models, 484, 486, 487
Deep-sea storms, 35 Dispersant exposure, 448
Deep-sea water anoxia, 508 Dissemination, 39, 467, 473–476, 478, 479
Deep-water benthos, 115, 214 Dissolution, 17, 19, 23, 74, 111, 462, 518
Deep-water bottom trawling, 538 Dissolved compounds, 392
Deep-water formation, 98, 105, 195, 198–200, 209, 507, 510 Dissolved inorganic carbon (DIC), 96–98, 100, 103, 406, 442, 459, 460
Deep-water giant oysters, 19 Dissolved inorganic compounds, 458
Deepwater Horizon, 465 Dissolved inorganic nutrients, 313
Deep-water organisms, 360, 366 Dissolved organic matter (DOM), 396, 456, 458–460
Deep-water renewal, 507, 508 Dissolved oxygen, 195, 197, 198, 267, 450
Deep-water ventilation, 47, 48, 98 Dissolved Inorganic Nitrogen (DIN), 204
Defence, 406 Dissolved inorganic phosphorous (DIP), 103, 104, 204
Degassing processes, 267 Distribution∗, 5, 15, 31, 51, 72, 100, 109, 157, 173, 192, 214, 245,
Deglacial, 51, 57–60, 78 249, 253, 265, 271, 285, 297, 336, 359, 378, 391, 407, 425,
Deglaciation, 5, 57, 59, 62, 78, 104, 165, 365 473, 488, 491, 502, 510, 519, 535
Degradation, 41, 287, 347, 351, 398, 513, 514, 531, 537 Distributional range, 9, 68, 229, 271, 279
Degraded, 16, 20, 117, 314, 339, 396 Disturbances, 109, 117, 258, 312, 346, 347, 378, 397, 405, 410, 417,
Demersal, 296, 298, 312, 319, 327, 488 428, 448, 452, 455, 513, 535, 539, 542
fisheries, 341, 342, 536 Diversified/diversification, 73, 74, 76, 137, 143, 379, 405
Demographic unit, 359 Djibouti banks, 297, 298
Demography/demographic, 3, 7, 10, 287, 358–362, 366, 423–431, 495 DMS, 379
Demosponges, 313, 388 DNA, 132, 142, 150, 364, 366, 380, 381, 387, 388, 485, 488, 521
Denaturing gradient gel elecrophoresis (DGGE), 379–384, 387, 388 DNA-barcoding, 141
Dendritic, 286 Downcanyon flows, 292
Dendrochronology, 412 Downward cascading, 196
Dense bottom currents, 35 Downwelling, 207, 384, 415
Dense shelf water cascades/dense water shelf cascades, 207, 237, 285, events, 195
286, 415, 418 Dragon Mound (DM), 62, 63
Dense water cascades, 195 Dredged samples, 20, 379
Dense water formation (DWF), 196, 197, 207–209, 507 Dredges, 20, 21, 31, 32, 91, 116, 117, 165, 184, 214, 226, 273, 274,
Densification, 198, 200 346, 359, 378, 379, 437
Density(ies) Drifters, 495
anomaly, 198, 200–203, 207, 208 Drillcoring, 22
band, 394 Drill cutting, 416, 464, 465
layers, 201–203, 409, 462 Drilling, 10, 17, 22, 23, 25, 47, 58, 464–465, 479
Department of Environmental and Earth Sciences, 68 Drivers, 5, 31, 32, 61, 64, 168, 209, 266, 357–369, 411, 415, 419, 428,
Depocenters, 48 484–491, 495, 513
Desiccation, 47 Drop-camera, 157, 162
Desmophyllum-limestone, 19 Dune sands, 48
Desmosponges, 162, 262, 263, 313 DyMiCo active sand bed filter, 452
Destruction, 257, 351, 461, 483, 537 Dynamic energy budget (DEB), 455
Destructive, 20, 41, 214, 234, 267, 346, 441, 455 Dynamic height and Sea Level Anomaly (SLA), 197
Detrital particles, 393 Dynamics
Detritivores, 460 barrier, 203
Detritus, 216, 336, 392, 440 current regimes, 39, 41
DGGE, see Denaturing gradient gel elecrophoresis Dysoxic, 52
Subject Index 563
E Embryo, 339, 345, 437, 461, 486–488

Early Holocene, 5, 42, 57, 59, 62, 67, 78, 196, 265 Embryogenesis, 399
Early life stages, 325, 338, 350 EMDW, see Eastern Mediterranean Deep Water
Early-Middle Pleistocene, 20, 75–76 Emerged coral deposits, 51, 54
Early mineralisation zones (EMZ), 97, 408 Emilia Romagna, 74
Early Pleistocene, 15, 16, 19, 52–54, 67–70, 75–77, 417 Emission scenario, CO2, 520
Early Pliocene, 47, 48, 75 Empiric, 100, 103, 437, 489, 493, 495
Early taphonomy, 17 Empirical calibration equations, 95
Early Tortonian, 501 EMT, see Eastern Mediterranean Transient
Earthquake, 168, 500, 503 Enarete Seamount, 219, 224
East Cabliers bank, 58, 59 Encounter protocols, 540, 542
Eastern basin, 36, 41, 42, 76, 78, 80, 117, 122, 196, 200, 201, 203, Encrusters, 20, 25, 324
207, 228, 234, 319, 327 Encrusting desmosponges, 313
Eastern Betics, 48 Encrusting fauna, 20
Eastern Florida, 341, 345, 348, 349 Endangered, 159–161, 164, 251, 254, 428, 537, 538
Eastern gateway, 503 Endemic, 6, 130, 140, 141, 149, 215, 361
Eastern Intermediate Water (EIW), 197 species, 132, 138, 149, 315, 413, 423
Eastern Mediterranean circulation cell, 198 Endodermal layer, 406
Eastern Mediterranean Deep Water (EMDW), 98, 105, 197–199, 508 Endofauna, 327
Eastern Mediterranean Transient (EMT), 199, 508, 510 Endolithic, 407
Eastern Melilla Coral Province, 76 Endosymbionts, 379
East Melilla (EM) Energetic, 293, 396, 397, 415, 418, 426, 462, 525, 533
province, 58, 59 Energy
seamounts, 220 acquisition, 393, 444, 455
Ebro Delta, 232 allocation, 524
EBSA, see Ecologically and Biologically Significant Marine Areas budget, 458, 459, 524
Echinoderms, 76, 253, 278, 280, 281, 295, 307, 308, 320–322, 448 storage, 406
Echinoid, 18, 161, 162, 277, 307, 314, 320–322 Energy-limited ecosystems, 396
Echiurid, 318 Engineering CWC bioconstructions, 68
Echosounders, 159, 184 Entangled, 247, 293, 345–347, 359, 442
Ecological crisis, 47–49 Environmental changes, viii, 41, 53, 59, 60, 78, 104, 358, 368, 391,
Ecologically and Biologically Significant Marine Areas (EBSA), 165, 393, 405, 406, 415, 419, 423, 444, 464, 519, 526
281, 537 Environmental factors, 7, 23, 235, 267, 383, 396, 397, 399, 405,
Ecological-Niche Factor Analysis (ENFA), 182 416, 417
Ecological niches, 78, 367, 379, 406, 419 Enzymatic, 406
Ecological patterns, 158 Enzyme activity, 396
Ecological time scale, 384 Epibathyal environments, 18
Ecological turn-over, 17, 20, 23 Epibenthic, 196, 337, 340
Ecology, v, viii, 7, 8, 10, 25, 80, 132, 140, 148, 175, 226, 233, 237, Epibionthic, 318
273, 281, 358, 363, 373, 377, 383, 384, 393, 399, 406, 437, Epibionts, 140, 258
461, 467, 475, 488, 515, 519 Epibiosis, 346
Economic importance, 427 Epibiotic species, 232
Ecophysiology, 391–399, 436, 437, 455 Epitoniid, 319
Ecosystem-based fishery management, 245, 351 Epoxy, 450, 453, 454
Ecosystem engineer, 61, 221, 245, 251, 399, 406, 416, 475, 518 Equilibrium depth, 200
Ecosystemic services, 15 Eratosthenes Seamount, 32, 196, 205, 206, 257, 515, 541
Ecosystem resilience, 398 Erect, 148, 245, 247, 324
Ecosystem services, 296, 513, 514, 535, 537 Erosional bedforms, 37
Ectodermal layer, 406 Erosional contourite features, 35
Ectotherm, 394 Erosive, 41, 165
Eddies, 35, 195, 200–203, 207, 485, 490 Eruptions, 267
Eddy fields, 202, 490 Erythraean species, 513–515
Effective management, 347, 351 Escarpments, 17, 19–23, 52, 79, 85, 92, 216, 218, 224, 225, 234, 253,
EFH, see Essential Fish Habitat 265, 272, 277, 278, 297, 325, 327, 338, 485, 490, 492, 493, 535
Egg Esquine bank, 192, 194
capsules, 338, 339 Essential Fish Habitat (EFH), 8, 312, 351
masses, 232, 335, 345 Estuarine, 491, 507
Eggcases Ethanol, 453, 454
cephalopods, 232 Ethic, 359
sharks, 232, 250, 337, 345 Ethology, 319, 327
Eigenvalue, 425, 426 EU Habitats Directive, 160, 161, 254, 263, 538
El Arraiche field, 265 Euler, 424
Electrical conduction, 436 Eulerian models, 492
Electrical disturbances, 397 EUNIS, 185
Electrician cutters, 454 Euphausiids, 319, 343, 350
El Idrissi Bank, 220, 232, 338 Eurasia, 499–501, 503
564 Subject Index
Eurasian plate, 499, 503 Faunistic, 295, 299, 312, 319, 327
Europe, vii, 32, 110, 147, 150, 168, 185, 474, 501 Feather-like, 146, 147, 233
European climate, 508 Fecundity, 398, 425, 426, 428–430, 455, 486, 489
European Marine Observation and Data Network (EMODnet), Feeding
175, 196 cycles, 410
European Union (EU), x, 11, 293, 328, 358, 365, 467, 475, 479, 538, ecology, 226, 437
539, 542 efficiency, 456, 466
Euryarchaeota, 387, 388 grounds, 9, 271, 341
Euxinic black shales, 48 habitat, 336–338, 340–344
Evaporation, 8, 36, 195, 198, 200, 206, 491, 507–510, 518, 519 metabolism, 226
Evaporite deposition, 48 Felt filter bag, 447
Evaporites, 47 Femto laser ICP-MS, 104
Evaporative marginal seas, 509 Fertile, 42, 429, 486
EVENT-DEEP, 160, 168 Fertilisation, 399, 460–461, 486–488
EVENT-SHELF, 160, 168 Fibreglass, 449
Evolution, 6, 8, 16, 47, 48, 51, 78, 80, 112, 115, 141, 358, 359, 361, Fibro-prismatic, 405
366, 369, 373, 375, 405, 413, 417, 419, 426, 466, 499–503 Fibrous aragonite (FA), 97, 103, 104
Evolutionary, 125, 131, 132, 357, 358, 360, 363, 365–369, 373, Filamentous algae, 466, 467
375, 383 Filicudi banks, 219, 224
time scale, 483, 484 Filtered seawater, 412, 438
Excavating sponges, 315 Filter-feeding invertebrates, 345
Exclusive Economic Zones (EEZ), 159, 537 Filtration units, 440, 442, 462
Exhibition, 438, 439, 443, 450, 466, 467, 474 Fine-grained siliciclastic deposits, 71, 75
Exhumed, 262, 267 Fingerprints, 185, 377, 379, 382, 384, 387, 388
Expeditions, vii, 3, 4, 32, 105, 115–117, 149, 165, 238, 266, 328, 391, FISH, see Fluorescence in situ hybridization
438, 515 Fish
eXpendable BathyThermographs (XBTs), 196, 197 abundance, 338, 340, 344
Experimental design, 443, 444, 462, 463, 520–525 diversity, 325, 327, 338, 341
Experimentation, 437, 440, 441, 443, 445, 454–467, 531 stock, 346, 540
Exploration, 4, 5, 7, 22, 25, 32, 35, 47, 115, 117, 149, 158, 165, 174, Fisheries, 9, 31, 168, 219, 237, 255, 285, 296, 320, 336, 346, 347, 360,
184, 191, 214, 215, 219, 221, 226, 237, 245, 249, 257, 259, 378, 384, 468, 475, 479, 514, 519, 535, 536, 538–542
271, 272, 281, 285, 291, 297, 317, 327, 346, 358, 365, 475, Fisheries Management Zone, 253, 254
476, 479, 518, 536, 537, 542 Fisheries Restricted Area (FRA), 165, 312, 346, 347, 351, 540, 542
Exposure time, 111, 520, 524, 531 Fishermen, 217, 249–251, 257, 259, 477
Extant, 16, 18, 19, 25, 31, 32, 41, 67, 68, 73, 77, 115, 131, 132, 135, Fishing activities, 147, 162, 214, 232, 245, 249, 257, 258, 346, 347,
136, 148, 368, 373 350, 351, 519, 536
Extensional ridges, 163 Fishing discard, 232, 247
Extensional settings, 261, 265–266 Fishing grounds, 232, 251, 293, 536
Extension rates, 393 Fishing impact, 214, 247, 250, 335–351
Extinction, 48, 51, 53, 67, 78, 79, 92, 165, 214, 368, 369, 417, 426, Fishing lines, 194, 219, 292, 346, 347
503, 539 Fishing operations, 32, 226
Extinct species, 52 Fishing vessels, 437, 540
Extracellular, 396, 406, 407, 416 Fission, 454
Extracellular mucus (EMS), 407 Fissurellid, 319
Extrusive events, 267 Fissures, 19, 490
Fixed point stations, 196
Fjords, 11, 15, 93, 97, 103, 336, 380, 381, 383, 395, 427, 447, 452,
F 462, 486, 487
Facies, 36, 39, 41, 75, 76, 87–92, 111, 112, 131, 137, 138, 147, 158, Flabellate, 142, 249, 313
161, 165–167, 176, 191–193, 214, 218, 220, 230, 234, 316, Flanks, 63, 157, 160–162, 165, 166, 185, 191, 216, 218, 219, 228,
318, 320, 338, 347, 538, 539 232, 262, 267, 272, 276, 287, 291, 417, 490, 535, 536
Facultative, 322, 335, 350, 487 Flexible colonies, 324
False chimaeras, 221 Float data, 204
Fan-like, 138, 229 Floatstones, 75
FAO, 347, 425, 475, 477, 538, 540–542 Flourishing phase, 51
Fatty acid-lipid, 392, 393 Flow
Fatty acids, 393, 395, 453, 459, 467 rate, 443, 445, 449–451, 453
Fault escarpments, 52 speed, 196, 392, 453, 456, 457
Fault scarps, 163, 165, 501–503 Flow-through system, 447, 451, 452, 457
Fauna, 3–8, 10, 11, 18–20, 51, 53, 54, 74, 76, 79, 115, 116, 121–123, Fluids, 7, 99, 102, 232, 261, 263, 265–267, 464, 467, 492,
126, 127, 129, 131, 132, 136, 137, 141, 144, 148–150, 189, 499, 526
191, 194, 213, 215, 219, 227, 233, 245, 249, 250, 253, 254, Fluid venting provinces, 265
258, 259, 261, 262, 272, 274, 276–278, 280, 281, 295–328, Fluid venting submarine structures (FVSS), 7, 261–263
336, 337, 340, 342, 347, 349, 365, 367, 377, 378, 384, 405, Fluorescence, 160, 162, 380
406, 413, 419, 439, 458, 464, 467, 489, 491, 535, 540 Fluorescence in situ hybridization (FISH), 310
Faunal community, 57 Fluorochromes, 412
Subject Index 565
Food Gas
capture, 519 exchange, 440
flux, 281 prospection/prospecting, 378, 384, 535
particles, 36, 39, 40, 61, 261–263, 272, 281, 392, 396, 447, 451, Gassy sediments, 267
453, 456, 461 Gastropods, 21, 22, 148, 263, 296, 305, 311, 318, 319, 327, 466, 467
sources, 162, 311, 378, 384, 391–393, 448, 451–453, 456, 459, Gastrulation, 488
460, 519 Gateway, 47–49, 257, 499, 501–503
supply, 51, 158, 235, 262, 311, 349, 350, 384, 397, 399, 416, 456, Gazul, 263, 297, 298, 311, 313, 314, 317, 322, 325
522, 536 Gene accC, 388
webs, 399, 513 Gene expression (GE), 455, 464, 521, 522
Food-rich areas, 393 Gene flow, 357–359, 361, 363, 367, 373, 430, 488, 491
Foraging, 344, 350, 461 blockage, 485
Foraminifera, 18, 22, 49, 76, 103, 161, 451 General Fisheries Commission for the Mediterranean (GFCM),
Foraminifers, 17, 23 165, 232, 312, 428, 537, 540–542
communities, 48 Generalists, 342
Forecasts/forecasting, 209, 405, 406, 413, 423, 424, 426, 428, 430, Generalized Linear Models, 182
431, 444, 491–493, 495 Generations, 6, 24, 42, 96, 346, 357, 358, 367, 407, 458, 479, 484,
Forest, 125, 180, 213–215, 218, 219, 228, 230, 231, 237, 249–251, 486, 489, 493, 536
253, 298, 316, 336, 338, 339, 343, 346, 359, 472, 473 Generic species, 493
Forest-forming, 213, 214 Genes, 125, 140, 148, 357–359, 361, 363, 366, 367, 373, 382, 383,
Forlì, 74 385, 387, 388, 430, 455, 464, 485, 488, 491, 520–522
Formentor Cape, 287 Genet, 359, 454, 485
Fossil Genetics
coral legacy, 115 diversity, 131, 357, 359, 360, 363, 368, 398, 399
CWC occurrences on-land, 68 isolation, 143
extant-type CWC habitats, 16, 18 markers, 360, 366, 367, 485
organisms, 16 pattern, 357–369
scleractinian, 80, 92 plasticity, 382
Fossilisable, 16, 20 profile, 357, 382
Fossilised biocoenosis, 21–22 signature, 360
Fossil record, 5, 7, 17, 48, 67, 74, 97, 143, 148, 150, 267 units, 358, 369
FRA, see Fisheries Restricted Area Genome, 123–125, 132, 358, 366–369, 388
Fragile, 135, 257, 292, 293, 378, 454, 466–467, 473, 475, 479, Genomics, 366–368, 375, 382, 484, 488
515, 537 Genotypes (GT), 358–360, 362, 454, 521, 522
Fragment/fragmentation, 17–19, 23, 24, 31, 59, 61, 62, 64, 69, 71, 74, Geo-acoustic, 157, 158
75, 80, 91, 92, 95, 98, 104, 109, 110, 130, 164–166, 258, 267, Geochemical proxies, 5, 23, 54, 73, 95–97, 100, 104, 406, 410, 412
273, 276, 278, 279, 281, 315, 323, 358, 359, 387, 398, 399, Geochemical signals, 23, 95–97, 99, 100, 104, 412
407, 408, 411, 412, 426, 436–438, 441, 445, 449, 451, Geodynamical processes, 499–503
453–455, 459–462, 465, 485, 488, 520, 531 Geodynamics
Frame-building, 5, 17, 53, 54, 67–71, 74–80, 213–215, 228, 315 evolution, 16, 115
ability, 214 reconstructions, 20
Framestones, 21, 22, 24, 87–89, 324 Geographical, 6, 8, 10, 68, 135, 148, 194, 228, 247, 249,
Framework collapse, 417 359, 361, 368, 378, 393, 426, 451, 486, 487, 489,
Framework expansion, 417 513, 536
Free amino acids, 378, 383, 392 Geographical areas, 6, 213, 486
Free-living, 125, 135, 136, 142, 147, 149, 360, 378 Geographic coordinates, 68, 359, 361
Freeze-thawing cycles, 387 Geographic Information System (GIS), 175, 177, 181, 192, 540
French canyons, 219, 230, 232, 234 Geo-habitats, 158
French continental shelf, 191 Geolocalised, 191, 193
French deep-sea canyons, 191–194 Geological dredges, 20
French margin, 502 Geological hazard, 35
French submersible expeditions, 116 Geological record, 15, 51, 360
Fresh Atlantic Water, 507 Geological surveys, 257, 343
Freshwater, 8, 200, 447, 459, 491, 507–510, 518, 525 Geological time, 5, 73–77, 79, 221, 285
Full-coverage maps, 157, 162 Geologic features, 158
Functionality, 7, 10, 11, 121, 195, 457, 458, 485 Geomorphic features, 159, 285, 312
Fungi, 17, 18, 417 Geomorphology(ies), 157, 159, 161, 163, 180, 336, 392
Future climate scenarios, 11, 417, 436 Geomorphometry, 175
FVSS, see Fluid venting submarine structures Geophysical
data, 167, 173, 184
seismic, 47
G Georeferenced colonies, 359
Gallipoli escarpment, 216, 225 Georeferenced map, 68, 80
Gamete quality, 398 Geo-referenced successions, 22
Gametes, 144, 358, 398, 452, 460–461, 487 Geosphere, 499
Gammaproteobacteria, 379–383 Geosphere-hydrosphere, 499
566 Subject Index
Geostrophic Ground-truth/ground-truthing, 158–160, 162–164, 166, 177, 180–182,

balance, 163, 197, 236 184, 185, 267
turbulence, 202 Growth
GEOTRACES, 103 modelling, 408–409, 413, 424
GES, see Good environmental status patterns, 405–419, 436
GFCM, see General Fisheries Commission for the Mediterranean rate, 9, 97, 100, 104, 224–228, 232, 247, 251, 262, 351, 393–395,
Ghost fishing, 346 399, 405, 410–419, 424, 426, 429, 431, 437, 441, 454, 455,
Giant coral mounds, 16 462, 524, 531, 536, 539
Giant elongated drifts, 37 Guadalquivir diapiric ridge, 265
Giant oyster, 19, 24, 218, 315, 322 Guadiaro submarine canyon, 287
Giant red shrimp, 320 Gulf of Alaska, 343, 344, 348, 349
Gibraltar Gulf of Aqaba, 406
gateway, 47, 49, 501, 503 Gulf of Cádiz (GoC), 39, 149, 261, 263, 265, 267, 295, 297–300,
strait, 36, 48, 105, 125, 142, 149, 195, 198, 201, 209, 214, 221, 303–305, 311–313, 316–319, 322, 324, 325, 327, 328, 360,
222, 232, 237, 247, 273, 279, 287, 297, 298, 311, 317, 323, 365, 366
324, 327, 365, 499, 507, 508 Gulf of Genoa, 322
Gibraltar Arc (GA), 500, 501, 503 Gulf of Lion (GoL), 4, 7, 9, 32, 33, 37, 196, 198, 207, 216, 219–220,
Gillnets, 346 223, 226, 227, 229, 230, 232, 234, 237, 273, 279, 281, 286,
GIS, see Geographic Information System 301, 302, 307, 311, 313, 347, 361, 406, 407, 411, 412, 415,
Glacial period, 53, 57–59, 79, 312, 392 416, 418, 438, 444, 507, 542
Glass, 160–163, 438, 443, 461, 464 Gulf of Mexico (GoM), 36, 267, 342, 345, 348, 349, 379, 380, 382,
Gliders, 196, 202, 204, 205 393, 396, 406, 411–414, 418, 427, 438, 441, 448, 465, 476,
Global change, 9, 10, 374, 391, 396, 406, 419, 467, 479, 513, 518, 477, 487, 490, 494, 514, 521, 524, 537
519, 525, 533 Gulf Stream, 490
Global climate change, 440, 517–526 Gullies, 291
Global environmental change, 405, 419
Global ocean intermediate layer, 207
Global overturning circulation, 507, 510 H
Global scale, 173, 182, 209, 296, 455 Habitat Area of Particular Concern, 341
Global warming, 117, 378, 384, 417, 418, 437, 440, 455, 510, Habitat(s)
517, 518 builders, 6, 121, 125, 141, 145, 149, 540
Global water cycle, 509 complexity, 262, 267, 298, 311, 312, 336, 346
Glycoproteins, 406 destruction, 483
Gnawing marks, 18 formers, 214, 232
GoC, see Gulf of Cádiz heterogeneity, 157, 298
GoL, see Gulf of Lion loss, 368, 513
GoM, see Gulf of Mexico mapping, 6, 9, 11, 23, 25, 157–168, 173–186
Gondola slide, 217, 225 models, 7, 237, 417
Gonochoristic, 398 Habitat-building, 6, 121, 125, 141, 145, 149, 540
Good environmental status (GES), 161, 185, 542 Habitat-forming species, 122, 130, 147, 148, 231, 249, 253, 254, 298,
Gorgonians, viii, 6, 7, 48, 74, 140, 141, 143, 149, 159–162, 193, 219, 311, 538
245–247, 249, 250, 253, 261, 292, 311, 315–318, 321, 326, Habitat-forming taxa, 253
337, 338, 342, 344, 345, 347–349, 384, 388, 413, 438, 444, Habitat-specific, 158, 184, 388
445, 447, 450, 451, 453, 455, 473, 487, 513, 515, 535, 536, Habitats Directive, 160, 161, 254, 263, 538, 539
538, 541 Habitat suitability model (HSM), 173, 181–183, 185, 207
Governance, 535, 542–543 Halocline, 462
Governments, 10, 251, 281, 293, 424, 474, 475, 477, 542 Handbook, 9, 436
GPS, 191, 359, 501, 503 Handling stress, 520
Grabbing, 76, 79 Hannoun, 32
Grabs, 91, 177, 178, 184, 214, 273, 286, 361, 377, 437 Hard-bottom habitats, 214, 313
Gradual, 208, 490, 531 Hard bottoms, 52, 75, 76, 121, 125, 130, 135, 136, 141, 149, 185,
Grain size, 19, 37, 38, 41, 184 213–215, 220–233, 250, 253, 261–263, 298, 311, 313, 315,
Gravels, 87–92, 161–163, 185, 292, 449 317, 319, 322, 325, 347, 539
Gravid, 335, 338, 344–346 Hardgrounds, 18–21, 23, 25, 39, 42, 62, 91, 92, 164–166, 176, 179,
Gravity coring, 22, 76, 79, 267 217, 221, 230, 250, 286, 315, 337, 339
Grazer, 320 Hardness, 158
Grazing rates, 396 Hard substrate, 15, 18–20, 22, 25, 48, 74, 85, 92, 116, 125, 163, 175,
Great Barrier Reef, 384 176, 184, 185, 214, 258, 259, 261–263, 267, 272, 277, 298,
Greece, 19, 53, 77, 257, 259, 297 315, 318, 320, 342, 363, 399, 453, 502
Greek islands, 15, 18, 92 Harmful, 443, 452, 466, 513
Greenhouse gas, 511, 517 Harvesting, 296, 425, 428
Greenpeace, 475 Hatton Bank, 340, 341, 541
Gregarious, 16, 68, 70, 77, 363 Hawaii, 413
Grey-Level Co-Occurrence Matrix (GLCM), 162 Headscarps, 163
Grid cells, 491 Health, 184, 378, 391, 392, 398, 405, 460, 461, 466, 467
Subject Index 567
Heat Hydrodynamics
exchange, 450, 518 forcing, 285, 456
sequestration, 518 simulations, 197
Heat and salt treatment (HEATSALT), 387 Hydrodynamism, 39, 322
Heavy dredges, 116 Hydrogen, 518
Hebrides Terrace Seamount, 341 Hydrography, 167, 195, 201, 349
Hellenic Arc off Crete, 85 Hydroids, 148, 231, 314, 316, 317, 327, 341, 345, 349
Hellenic trench, 85–93 Hydrothermal vents, 379
Hellenic Trough, 17, 21 Hydroxylapatite inclusions, 103
Helvetian, 73 Hydrozoans, 52, 123, 292, 315, 317, 341
Hemipelagic foraminifera-rich sandy mud, 267 Hypersaline, 510
Hemipelagic Sant’Agata Fossili, 48 Hyperspectral cameras, 185
Hermaphroditism, 398, 399 Hyperspectral imager, 173, 185
Hermatypic, 73, 388 Hyperspectral images, 173, 185
HERMES, 4, 105, 168, 238, 328, 467, 475, 533 Hyposaline, 510
HERMIONE, 4, 105, 238, 328, 361, 467, 475, 533 Hypoxia, 519
Hermit crabs, 292
Heterotrophic, 262, 455
Hexacorallia, 122–132, 301, 541 I
Hexacorallian, 123, 124 Iberian-Provençal Basin, 324
Hexacorals, 450 Ibiza Channel, 207
Hexactinellida, 300 Ichnotaxa, 18
Hexactinellids, 313 Ierapetra, 201
Hexactinellid sponges, 262 Illa Negra, 291–293
High-definition visual tools, 159 Image analysis, 158, 180–182, 412
High energy environments, 233 Immune system, 378
High-latitudes, 100, 272, 367, 391, 487, 491 Impacts, 9, 10, 41, 48–49, 53, 62, 99, 138, 150, 159, 163–165, 173,
High quality food, 452 185, 191, 194, 209, 214, 232, 237, 247, 249–251, 258, 291–293,
High resolution bathymetry, 62, 159, 287, 291 335–351, 360, 363, 395, 399, 413, 416–418, 431, 437, 444, 454,
High salt content, 507 455, 462, 464–466, 474–476, 483, 499, 502, 503, 507–511,
High vulnerability, 518, 535 513–515, 517, 518, 524–526, 531, 535–537, 540, 542, 543
Hindcasts, 495 Incubation chambers, 397, 440
Hirondelle, 4, 32 INDEMARES, 160, 263, 311, 328, 467, 474, 475
Historical biology, 115 In-depth sequencing, 379, 388
Historical datasets, 96 Indian Ocean, 501, 503
Historical records, 31 Individual Based biophysical Models, 492, 493
Historical simulations, 509 Indo-Pacific, 74, 75, 137, 138, 412, 513, 514
Historical studies, 200 Industrial agglomerations, 508
History, vii, 3–8, 16, 31–33, 41, 49, 51, 64, 74, 80, 96, 104, 125, 142, Infaunal, 177
164, 213, 215, 226, 258, 358, 361–363, 365–367, 373, 399, Infestation, 466, 467
425, 426, 428, 431, 452, 483, 484, 486, 492, 493, 495, 502, Inlet, 443, 503
515, 517 Inorganic aragonite, 100
Holobiont, 378, 382, 384, 387, 389, 399, 459–460 Inorganic carbon, 96–98, 197, 406, 442, 459, 460
Holocene, 5, 20, 22, 41, 42, 51, 54, 57, 59, 60, 62, 67–69, 72, 76–79, Inorganic nutrients, 313, 411, 443, 521
95, 104, 117, 165, 196, 265–267, 363, 417, 491 In situ, 9, 19, 20, 100, 103, 145, 147, 204, 206, 271–273, 341, 344,
Holocene Climatic Optimum, 508, 511 345, 380, 388, 392–395, 405–407, 411–415, 417, 418, 435,
Holothuria, 320 436, 439, 441, 442, 451, 455, 458, 459, 461, 463, 465, 487,
Holothuroid, 320 488, 490, 493, 495, 520, 524
Home laboratories, 436–439 experiments, 9, 405, 411, 417, 418, 458, 520
Homing instincts, 493 Instantaneous fields, 202, 207
Homothermal, 53 Institut de Ciències del Mar, 445, 450, 453, 468
Homothermic, 122 Institute of Marine Sciences, 68
Hormones, 461 Instituto do Mar (IMAR), 445–447
Hotspots, 7, 8, 10, 11, 15, 31, 32, 168, 193, 197, 253, 261, 263, 285, Instrumental records, 96, 199
298, 313, 508, 519 IntCal 13 curve, 98
HSM, see Habitat suitability model Interglacial, 59, 78, 417
Human activities, 263, 398, 515, 535, 536, 538, 542 Intergovernmental Panel on Climate Change (IPCC), 11, 417, 418,
Human impact, 138, 150, 291 437, 444, 462, 518, 536
Human-induced disturbance, 513 Intergovernmental panels, 542
Human occupied vehicle (HOV), 191 Integrated Ocean Drilling Program (IODP), 17, 23, 39
Husbandry, 436, 442 Intermediate/bathyal waters, 98
HYbrid Coordinate Ocean Model (HyCOM), 490, 491, 495 Intermediate-depth water pH, 103
Hydraulic theory, 262 Intermediate layer circulation, 202, 203, 207, 208
Hydrocarbon Intermediate water(s)
drilling areas, 464 formation, 195, 197, 198, 200
exploration, 35 mass, 8, 59, 76, 97, 195–209, 265
568 Subject Index
Inter-mound, 52, 166 Kernel density plots, 493

Internal fertilisation, 399 Key habitat features, 214
Internal pH, 103, 396 Key oceanographic parameters, 95, 105
Internal tides, 287 Kinematic, 501
Internal waves, 35, 285 Kinetic effects, 99
International Guidelines for the Management of Deep-sea Fisheries, Kleptoparasite, 317, 318
538, 540 Knolls, 157, 265, 280, 342, 541
International Union for Conservation of Nature (IUCN), 122, 149, Knowledge transfer, 7, 473–479
160, 214, 232, 247, 251, 254, 259, 475, 536, 538 Krill, 450–452, 462
Inter-reef connectivity, 492
Intracellular, 409
Intraspecific variability, 74, 80, 531 L
Invasion debt, 515 Laboratory cultures, 489
Invasive species, 259, 483, 485 Laboratory model, 507
Inventories, 103, 121, 123, 126, 127, 129, 136, 141, 149, 150, 185, Laboratory of Marine Geology in Bologna, 117
254, 285, 287, 295, 369, 538, 539 Lacaze-Duthiers, H., 4, 32, 127, 129, 137, 143, 192, 193, 207, 219,
Invertebrates, 7, 9, 11, 16–18, 22, 115, 137, 237, 298, 311, 314, 318, 272, 286, 291, 297, 325, 336, 347, 361, 380, 381, 408,
335, 337, 340, 341, 345, 346, 350, 378, 454, 466 411–413, 415, 416, 418, 427, 444
In vivo, 214 La Fonera, 7, 193, 207, 222, 271, 272, 274–280, 286, 287, 291–293,
Ion homeostasis, 395 311, 315, 317, 322, 536
Ionian basin, 131, 143, 147, 202 Lago Mare, 48, 49
Ionian Circulation, 199 Lagrangian models, 492
Ionian Sea, vii, 6, 17, 21–23, 41, 42, 62, 92, 98, 100, 117, 147, 157, La Linea submarine canyon, 287
159, 163–167, 201, 203, 216–218, 221, 225, 226, 229, 230, Laminar, 48, 443, 453
232, 236, 258, 272, 273, 279, 296, 324, 337, 338, 361, 364, La Montagna, 19, 20, 69
365, 406, 411, 412, 438, 515, 542 Lander, 337, 338, 340, 458
Ionisation efficiency, 101 Landlocked basin, 499
Ion microprobe, 23 Land-ocean interaction, 492
IPCC, see Intergovernmental Panel on Climate Change Landscape connectivity, 358
Ireland, 22, 61, 351, 361–364 Langhian, 48, 49, 73, 501
Irish continental margin, 340 LAPMv2, 178
Ischia, 395 Lardos SW Hill, 18, 92
Isidid corals, 19 Large marine ecosystems (LMEs), 511
Island of Montecristo, 338, 347 Larvae, 8, 74, 221, 261, 262, 315, 319, 345, 357, 360–362, 398, 399,
Isobaths, 163, 191, 236 417, 426–430, 461, 462, 483–495, 513
Iso Cluster, 182 settlement, 261, 262, 399, 417, 486
Isolated colonies, 158, 193, 219, 272, 286 Larval behavior, 437, 462, 488, 493, 495
Isolation, 48, 49, 98, 143, 363, 373 Larval buoyancy, 430, 484, 488
Isopods, 453 Larval development, 461, 487
Isopycnal, 200–205, 207, 208 Larval dispersal, 228, 233, 238, 363, 373, 399, 461, 483, 488,
outcrops, 203, 208 494, 542
Isotherm, 201 Larval distribution, 393
Isothermal tank, 438, 439 Larval mortality, 489
Isotope, 10, 41, 48, 95–104, 378, 392, 393, 406, 412, 413, Larval movement, 484, 495
458–459, 521 Larval output, 426, 429, 486, 493, 495
Isotopic dating, 360 Larval pool, 486
Israel, 202, 514 Larval predation, 486
Istanbul, 503 Larval production, 460
Italy, 15, 16, 18, 20, 48, 49, 52, 53, 68–71, 73–75, 77, 79, 115, 207, Larval recruitment, 417
216, 218, 328, 337, 395, 396, 468, 490 Larval settlement, 263, 298, 399
IUCN, see International Union for Conservation of Nature Larval spread, 209
IUCN Red List, 214, 247, 251, 254, 538 Larval supply, 398
Larval swimming, 430
Larval traits, 430, 484, 485, 489
J Larval transport/larva transport, 235, 357, 430, 492
Jaubert plenum, 448 Laser ablation ICP-MS, 23, 96, 97, 103, 104
Jean Charcot, 32 Last Glacial Maximum (LGM), 85, 92, 104, 266, 357–362, 365, 367
Jewelry, 140, 250, 428 Late Glacial (LG), 52, 53, 58
Juvenile concentration, 337 Late Holocene, 59, 265, 267
Juveniles, 69, 133, 259, 337, 338, 344, 345, 350, 419 Late-maturing species, 486
Late Miocene, 5, 47, 150, 213
Latent heat loss, 507, 509
K Late Pleistocene, 15, 16, 20, 22, 23, 41, 52, 54, 67, 68, 70, 72,
Karpathos, 17–19, 52, 76, 85, 87–91, 225, 297, 515 76–77, 79, 96, 105, 117, 150, 163, 165, 196, 296, 360,
island, 19, 52 365, 515
Kephalonia Island, 297, 311, 325 Late Quaternary, 68, 100
Subject Index 569
Late Tortonian, 48 Local adaptation, 357, 396

Latitudes, vii, 35, 87–92, 107, 149, 203, 208, 272, 275, 322, 365, 367, Local biodiversity, 150, 281, 311, 405
391, 427, 487, 491, 518 Local fluxes, 313
Layer thickness, 200 Logachev Mounds, 341, 361, 541
Lazzàro, 18 Logistic equation, 424
Lebanon, 202, 259, 536 Longevity, 227, 251
Lecithotrophic, 399 Longitudinal axis, 410
Lecitotrophic larvae, 426, 430 Longitudinal lineations, 163
Les Moines canyon, 192–194 Long lines/longlining, 162, 214, 217, 232, 245, 247, 250, 293, 326,
Lethal, 394, 417 335, 337, 340, 341, 345–347, 351, 359, 536, 540, 541
Leuca, 74 Long-lived, 124, 150, 201, 484–486
Levant, 200, 509, 513, 515 species, 137, 413, 425, 426, 428, 485, 493
Levante Canyon, 223, 272, 273, 286 Long-term
Levantine basin, 5, 143, 236, 249, 259, 507, 508, 538 acclimation, 520
Levantine Intermediate Water (LIW), 5, 8, 31, 32, 35–37, 40–42, 98, changes, 41, 96, 197, 415, 503
99, 105, 195–207, 209, 213, 235–237, 253–254, 266, 312, 364, Loop Current, 490
365, 490, 491, 507–511, 542 Loss of tissue, 466
subducts, 201 Lotka-Volterra, 424
Levantine Mediterranean basin, 257, 259 Low oxygen, 76, 417, 440
Levantine Sea, 85, 195, 199, 201, 225, 259
Levins, R., 426
Levkos, 19 M
LG, see Late Glacial Macrocnemic, 137
LGM, see Last Glacial Maximum Macrofauna, 18, 109, 297, 298, 312
Libby Mean Life, 98 Macrohabitat, 164–167, 337, 340, 363
LIFE BaĦAR for N2K, 136, 138, 140, 218, 253–255, 314, 326, 339 Macromorphology, 131
Life history Macroorganisms, 68
critical habitat, 8, 335–351 Maërl beds, 245
stages, 164 Magnesium calcite, 405
traits, 358, 365, 425, 426, 428, 431, 483, 486, 493, 495 Magnetic island, 382, 384
Life span, 251, 399, 413, 415–417, 428, 429, 486, 489 Maintenance, 272, 298, 395, 396, 436–445, 448–453, 458, 461, 467,
Life-stage mortality, 484, 485, 489 468, 520, 533
Life stages, 325, 336, 338, 350, 426, 429, 491 Majorca, 287
Life table, 425, 428, 429 Málaga, 57, 136, 316, 328
Lifetime, 93, 485 Malta
Li-820 gas analyser, 447 coral province, 320, 322
Light, 5, 36, 131, 160, 327, 387, 393, 398, 409, 439, 444, 449, 452, Escarpment, 17, 21, 23, 224, 297, 325, 327, 338
459, 467, 499, 526 Graben, 253
Lightning, 3, 115 Trough, 253, 314, 326
Ligurian Sea, 143, 219, 223, 226, 229, 232, 234, 272, 273, 279, 286 Malta-Siracusa Escarpment, 21, 22, 77
Limestones, 15, 18–22, 74, 79, 116, 117 Maltese Islands, 230, 253, 254
Limpet gastropods, 22 Maltese waters, 7, 253–255, 427
Lindos Bay clay, 18 Malthus, T.R., 424
Linear extension rate, 393, 413, 414, 522 Management, vii, 7, 9, 80, 150, 157, 168, 173, 185, 194, 213, 245,
Linear growth rate, 411, 412, 455 247, 251, 259, 281, 287, 347, 351, 360, 365, 367, 384, 399,
Lines technique method, 99, 100 423, 425, 428, 448, 473, 478–479, 483, 535–543
Linnaeus, C., vii, 5, 11, 31, 85, 92, 214, 217, 219, 220, 228, 230, 232, Manipulation, 463, 531
235, 272, 301–307, 309–311, 374, 377, 513–515 Manned submersible, 4, 20, 22, 32, 177, 245, 286, 437, 438
Linosa Island, 24, 109, 111, 219, 311 Mantice Shoal, 223, 229
Lionfish, 259, 513, 514 Mantle, 502
Lipid(s) Mapping, 6, 9, 22, 157–159, 164, 165, 168, 173, 175, 176, 182–185,
droplets, 452 202, 285, 288, 296, 473, 540
food, 452, 459 techniques, 22, 157, 158, 184–185
signature, 392 Mapping European Seabed Habitats (MESH), 173
List of Marine Habitat Types, 254, 538 Marco Bank, 224, 229, 347
Lithification, 17, 20, 22, 39 Marginal, 491, 499
Lithology, 37, 184, 291, 490 sea, 51, 509
Lithosphere, 500–502 Mariculture, 513
Litter, 191, 274, 279, 293, 536 Marine biota, 499, 514
Live rock, 448 Marine calibration curve, 68, 70
Living colonies, 32, 57, 161, 216, 219, 221, 226, 276, 279, 281, 292, Marine carbonates, 101, 110
297, 318, 321 Marine Climate, 201
Living coral, 3, 31, 32, 62, 85, 117, 135, 166, 216, 298, 315, 340, 358, Marine debris, 340, 535
383, 407, 438, 439, 447 Marine litter, 191, 274, 279, 293, 536
LIW, see Levantine Intermediate Water Marine mineral resources, 537, 542
LMEs, see Large marine ecosystems Marine observatories, 10, 436
570 Subject Index
Marine policies, 535, 537–539, 542 Mediterranean Surface Water (MSW), 36

Marine pollution, 368, 378, 399, 513, 518, 526, 535, 536 MedSeaCan cruise, 191–194
Marine Protected Areas (MPAs), 179, 216, 233, 251, 253, 254, 365, Megabreccia, 18
369, 375, 441, 483, 488, 537, 539, 540, 542 Megafauna, 18, 262, 296, 297, 335, 336, 338
Marine Protected Areas Agency (AAMP), 441 assemblages, 319
Marine radiocarbon curve, 98 Meiofauna, 296, 312, 327
Marine realm, 47, 501 Melilla, 5, 32, 33, 37, 40, 42, 58, 59, 61–64, 73, 76, 111, 161, 220,
Marine reserves, 360, 514 221, 298, 311, 322
Marine seascape niche, 484 mounds, 59, 161, 220
Marine Strategy Framework Directive (MSFD), 185, 204, 238, 293, Melilla Coral Province (MCP), 76, 111, 298, 322
351, 542 Melting of glaciers, 518
Marine surface curve, 98 Melting of ice caps, 518
Marine technologies, 117 Members of industry, 542
Mari Siculo, 31 Membrane, 143, 409, 461
Maritime, 542 Memory effect, 101
sectors, 536 Mersa-Matruh Gyre, 202
Maritime Spatial Planning (MSP), 168, 542 MESA program, 474
Marking larvae, 483, 484 Mesenterial filaments, 407, 452
Markov Chain, 425 Mesenteries, 123, 124, 131, 137, 138, 148, 398, 407, 452
Marly, 74–76 MESH, see Mapping European Seabed Habitats
sediment, 18 Mesocosm, 447
Marmara, 143, 147, 225, 226, 246, 297, 363, 500, 501, 503 Mesoglea, 398, 406
Marmorito, 75, 79 Mesopelagic, 350, 387, 388
Marseille, 31, 32, 123, 137, 196, 272 Mesophotic, 10, 513–515
Mass flow controllers, 440 Mesoscale, 201, 274, 490
Massive species, 313 Mesozoic, 68, 163
Mass spectrometers, 96 Mesozooplankton, 392
Mass-wasting events, 93, 157 Messina Strait (MS), 20, 52, 75, 225, 232, 237, 303, 306
Mating, 335, 345, 361 Messinian evaporite deposition, 48
Matrix effects, 101 Messinian Salinity Crisis, vii, 5, 41, 47–49, 141, 213, 286, 365, 501,
Matrix populations models, 425, 426, 428, 429 508, 511
Maturation, 339, 461 Messinian stage, 74
Mature individual concentration, 337 Metabolic
Maturity, 228, 351, 399, 486, 487, 489, 490, 493 activity, 97, 395–397, 405, 459
Maximum entropy modelling, 182, 292 cost, 350, 395
Maximum Likehood classification, 182 functions, 393
Maximum Likelihood Classifier algorithm (MLC), 162, 166 plasticity, 382
MBES, see Multibeam echosounder bathymetry products, 459
MC-ICPMS, see Multi-collector inductively coupled plasma mass rate, 395, 487
spectrometry Metabolism, 226, 363, 384, 395, 397, 418, 442, 464, 520
MCP, see Melilla coral province Metacommunity theory, 384
MeBo, 22, 62, 64, 76 Metals, 406, 412, 458
MECCA, 441 Metapopulation, 366, 425–426, 430, 483, 484, 486, 488
Mechanical damage, 346 Meteor, 32, 96, 117, 328, 438, 440, 441, 453, 455
Mechanical disturbances, 397 Meteoric waters, 20
Mechanical filter, 438, 439, 443 Meteorology, 490
Mechanical impact, 232, 251 Methacrylat, 441, 450
Mechanical injuries, 346 Methane, 261, 262
Median Probability Age (MPA), 70, 540 Methane-derived authigenic carbonates (MDACs), 261–263
network, 485, 539, 540, 542 Methanogenetic limestones, 74
Mediterranean Methodologies, 7–9, 16, 23, 157, 159, 168, 173–186, 193, 271, 419,
basin, 3–6, 10, 15, 16, 18, 20, 23, 36, 41, 47–49, 67, 68, 76, 77, 79, 439, 460, 488
96, 98, 99, 115, 117, 121, 131, 132, 136, 138, 141, 143, Metrics, 175, 358, 493
147–150, 165, 167, 176, 185, 196, 214, 221–225, 227, 230, Micriticised sponges, 322
235, 249, 257, 259, 272, 273, 295, 296, 318, 322, 327, 328, Micritic limestone, 15, 21
360, 438, 490, 491, 499, 501–503, 507, 509–511, 515, Micritisation, 20
535–538, 540, 542 Microalgae, 452, 453, 461, 462
overturning circulation, vii, 96, 490, 507, 508, 510, 511 Micro-analytical techniques, 23
Red List, 160, 259 Microarchitecture, 17, 24, 75
Ridge, 261, 265 Micro-basins, 75
Mediterranean-Indian Ocean gateway, 501 Microbial
Mediterranean Marine Peace Parks, 165 abundance, 378
Mediterranean Ocean Forecasting System (MFS), 490, 491 communities, 11, 382, 388
Mediterranean Outflow Water (MOW), 39, 209, 298, 327, 365, 510 Microbiome, 377–379, 383, 384, 419
Mediterranean Strategy for Sustainable Development (MSSD), Micro-buildup, 77
537, 542 Microcarnivores, 319
Subject Index 571
Micro-density, 524 Monitoring, 10, 157–159, 168, 185, 191, 267, 351, 419, 435, 436,
Micro-drilling system, 97, 103 443–444, 457, 463
Micro-eddy, 493 Monopodial, 125, 227–228
Microenvironments, 377–379 Monopoli, 218, 225
Microfauna, 18, 461 Monotonic, 425, 429
Microhabitats, 295, 298, 313, 320, 327, 387, 490 Montebaranzone, 74
Microlayers, 409–410, 415, 416 Montegibbio, 74
Micromorphology, 19, 75, 131, 132 Montenegrin margin, 262, 324
Microorganism, 8, 68, 384, 387, 397, 438 Montenegrin slope, 286
Microplastics, 479 Montenegro
Microsatellite(s), 361–363, 366, 367, 373 coast, 217
sequence, 71, 361, 363 slope, 174, 178, 182
Micro-scale, 97, 103 Montepetra site, 74
Microstructure, 7, 17, 97, 100, 104, 131, 132, 405, 408–410, 463 Monterrey Bay Aquarium, 474
Micro-tidal conditions, 36 Monte Torre succession, 18
Microtomographic imaging, 19 Monthly lunar cycle, 415
Microtomography, 24 Moon light, 398
Mid-Atlantic Ridge, 61, 500, 541 Moorings, 176, 204, 205
Middle Pleistocene, 41, 42, 52, 75–77, 92, 167 MOOSE, 197
Mid-domain effect, 247 Moroccan coast, 62, 220
Mid-latitude, 35, 214 Moroccan margin, 59, 61, 221, 265, 266, 322, 360, 366
Mid-Term Strategy, 537, 542 Morphological analyses, 70, 123, 373
Migrate, 115, 487, 489–492, 501 Morphological plasticity, 373
Migration, 261, 262, 350, 357, 358, 360, 363, 365–367, 423, 484, 485, Mortality, 229, 293, 337, 394–395, 424–426, 429, 438, 464, 484–486,
487–489, 493, 500, 501, 503 489, 491, 493, 495, 524
Milankovitch, 41 Mosaic, 159, 160, 164–167, 178–180, 184, 185, 237, 359, 535
Millennia, vii, 17, 61, 62, 362, 406 Mosaicism, 359–360
Millennial, 41, 96, 227, 427 Motility behavior, 426, 430, 484
Mineral Mound(s)
exploration, 518 aggradation rates, 57, 59, 60, 62
extraction, 391 shape, 61, 63, 165
organisation, 524 Mouth, 123, 272, 274, 392, 461, 492
Mineralogical structures, 405 Move-on rules, 541, 542
Mineralogy, 18, 20, 405 MPA, see Median Probability Age
Mingulay, 384, 441 MPAs, see Marine Protected Areas
Reef, 110, 341, 345, 378–380, 382–384, 387, 412, 456 MSFD, see Marine Strategy Framework Directive
Miniature model ocean, 519 MSP, see Maritime Spatial Planning
Miniature ocean, 51, 197 MSSD, see Mediterranean Strategy for Sustainable Development
Mining, 10, 263, 447, 479, 518, 537 MSW, see Mediterranean Surface Water
Minorca Canyon, 287 Mucus, 378–381, 383, 384, 387, 388, 392, 393, 396, 397, 407, 438,
Miocene, 5, 16, 31, 47–49, 62, 67–70, 73–75, 77, 79, 143, 150, 159, 458–461
213, 363, 365, 500, 501, 503 production, 391, 397, 437, 439, 452, 460
Mississippi chambers, 451, 452, 456–458, 460, 465 Mud breccia, 261, 265–267
Mitigation actions, 476, 477 bottoms, 261, 317
Mitochondrial COI, 132, 137, 141, 258, 363 Mud diapirs, 7, 57, 261, 266
Mitochondrial DNA, 132 Muddy
Mitochondrial genome, 124, 125, 132, 366 bathyal bottoms, 232, 315, 319, 320
Mitochondrial markers, 132, 141, 367 bottoms, 219, 229, 232, 234, 247, 261, 277, 293, 311, 320, 338,
Mitochondrial molecular markers, 125, 363, 373–374 339, 346, 347, 350, 351
Mitochondrial nucleotides, 70–71 Mudstone, 75, 166, 167
Mixed bottoms, 298, 325 Mud volcanoes (MVs), 7, 23, 57, 58, 259, 261, 262, 265–267,
Moats, 35, 37, 42, 62–64 313, 541
Mobile fauna, 337, 378 Mudwave fields, 42
Mobile species, 292, 311, 426, 474 Multibeam echosounder bathymetry (MBES), 61, 175, 176, 178,
Model assumptions, 485 184, 185
Modeling, 24, 121, 195, 202, 214, 423, 425, 427, 430, 431, 483–486, Multibeam swath bathymetry, 157, 158
489–495 Multi-collector inductively coupled plasma mass spectrometry
Model run timespan, 492 (MC-ICP-MS), 100, 101
Mode of reproduction, 486–487 Multi-decadal, 96
Modern distribution, 15, 18 Multiple cohorts, 484, 487
Molds, 19 Multi-specific assemblages, 227
Molecular analyses, 8, 70, 125, 135, 137, 258, 357, 373 Muricidae-Coralliophilinae, 22, 311, 319
Molecular markers, 123, 125, 132, 137, 150, 363, 373, 374 Museum collections, 31, 48, 67, 68, 150
Molecular taxonomy, 122 Museum of Natural History of the Torino University, 49, 74, 80
Mollusks, 537 Mutualists, 377, 378, 383
Monaco, ix, 4, 191, 384, 439, 444–445, 455, 456, 468 Mysidacea, 307, 319, 416
572 Subject Index
N North western Mediterranean, 7, 145, 147, 271–281, 286, 291–293,

Nacreous, 405 320, 324, 361, 393, 407, 408, 412, 427
NanoSIMS, 104 Norway, 4, 17, 99, 110, 232, 340, 343, 351, 388, 396, 410, 413, 414,
NAO, see North Atlantic Oscillation 416, 417, 438, 452, 468
Natal organism, 485 Norwegian fjords, 11, 93, 336, 380, 381, 395
National, 159, 160, 204, 254, 287, 365, 538–540, 542 Norwegian shelves, 227, 340
Park Calanques, 194, 539 Norwegian University of Science and Technology, 436
Natura 2000, 253, 358, 365 Nova Scotia, 342, 345, 349, 412
Naturalist, 115, 479 NTIMS, see Negative thermal ionization mass spectrometry
Naturalness, 164–165 Nubbin, 407, 415, 441, 450, 451, 453–455, 457, 531
Natural refuges, 287 Nuclear histone H3, 258
Natural shelters, 285–287 Nuclear markers, 361
Natural substrate, 430 Nucleation, 265, 267, 406, 408, 409
NCM, see North Catalan margin Nucleus for European Modelling of the Ocean (NEMO), 491
NEA, see North East Atlantic Nudibranch, 319
Near-bottom currents, 281, 342 Numerical models, 197
Near-surface layers, 196 Numerical simulations, 200, 413
Negative geotactic, 399 Numerical studies, 195, 200
Negatively buoyant, 488, 490, 492 Nursery
Negative thermal ionisation mass spectrometry (NTIMS), 101 area, 325, 338, 345, 347, 536
Nematocysts, 392, 393, 453 habitat, 325, 336–339, 344–346, 406
Nemerteans, 327 Nutricline, 204
NEMO, see Nucleus for European Modelling of the Ocean Nutrient
NEMOMED12, 490, 495 concentration, 23, 103, 416, 467
Neodymium, 42, 95 content, 95–97, 104
Neogene, 16, 53, 67, 68, 79, 501 inventory, 103
Neptunian dykes, 19 proxy, 95, 98, 103–104
Nested, 335, 345, 359, 491 replenishment, 443, 507
Net(s), 35, 165, 195, 202, 206, 245, 247, 250, 258, 259, 274, 279, 281, supply, 267, 392, 417
293, 346, 347, 378, 411, 460, 461, 490, 491, 508, 518, 536 Nutrient-rich, 285, 391, 427
evaporation, 8, 200, 507–510 Nutrition, 267, 311, 378, 383, 391, 393, 395, 459, 466
Network, 163, 286, 291, 298, 338, 358, 361, 362, 364, 365, 368, 406, Nutritional needs, 393
425, 426, 430, 483, 485, 488, 539, 542 Nystiellid, 311, 319
Neutral genetic diversity, 360
Neutrally buoyant, 365, 461, 488, 490, 492
New millennium, 116–117 O
Next-generation data sets, 382 Observational studies, 197, 509
Next generation sequencing (NGS), vii, 357, 358, 366, 367, 369 Observers, 192, 346, 479, 540
Nice canyon, 192, 193 Occurrence, vii, 5, 6, 8, 9, 15–23, 25, 32, 35, 37, 41, 42, 48, 57–59,
Niche, 78, 265, 267, 298, 367, 379, 406, 419, 484 61, 62, 67, 68, 73–75, 77–80, 85, 86, 91–93, 115, 121, 122,
Nile Deep Sea Fan, 266 132, 135, 138, 139, 142, 146–148, 150, 157, 159, 161–163,
Nile River, 491, 509 165, 166, 183, 186, 191–192, 194, 213–238, 250, 251, 259,
Niskin bottles, 438, 440 263, 265–267, 271–281, 285, 286, 292, 296–298, 313, 317,
Nitrates, 443, 451, 452, 459, 460, 466, 522 319, 320, 322, 325, 328, 335, 337, 338, 340, 345, 347, 350,
Nitrifying bacteria, 443, 460 359, 360, 363, 383, 407, 499, 502, 503, 510, 511, 514, 525,
Nitrogen cycling, 458–460 535, 537, 540
Nitrogen isotopic signature, 392 Ocean(s)
Nitrospirae, 382 bottom, 199
NOAA, 474, 475 climate, 510
Non-destructive methods, 411 currents, 197, 357, 373, 426, 430, 485, 490, 492, 495, 518
Non Governmental Organizations (NGOs), 475–477, 542 forecast data, 491
Non-indigenous species (NIS), 10, 513–515 forecasts, 491, 492
Non-marine cements, 20 level, 384
Non-native species, 489 NutritionTM, 391
Nora Canyon, 21, 219, 226, 286, 297, 321, 324, 325 salinity field, 509
North Adriatic Deep Water, 235 ventilation, 96
North African climate, 508 warming trend, 518
North Anatolian Fault (NAF), 500, 503 Oceana, 126, 127, 130, 131, 135, 136, 138–140, 143, 145, 151,
North Atlantic Oscillation (NAO), 509 159–161, 165, 254, 314, 321, 326, 339, 351, 474, 475,
index, 509 477–479, 536, 539
North Carolina, 342, 345, 349 Ocean acidification (OA), 9, 10, 23, 96, 103, 117, 159, 226, 363, 374,
North Catalan margin (NCM), 272–274, 281, 291, 293 377, 384, 395, 399, 418, 440, 441, 447, 448, 460, 462–464,
North East Atlantic (NEA), 53, 148, 149, 215, 285, 335, 336, 479, 517–526, 531–533, 535–537, 542
340–341, 344–345, 348, 349, 357, 361, 365, 367, 396, 406, Oceana Ranger, 253
414, 462, 475, 486, 487, 489, 510, 541 Ocean Floor Observation Protocol (OFOP), 177–178
Northeast Pacific, 335, 336, 343–345, 348, 349 Oceanic lithosphere formation, 501
Subject Index 573
Oceanographic expeditions, 31, 165 Outer insular shelf, 257

Oceanographic processes, 6, 35, 157, 158, 197, 293 Outlet, 503
Oceanographic vessels, 4, 436 Outreach, 473–479
Oceanward, 501 Overexploited, 428
Octocorals, 6, 16, 19, 22, 25, 52, 75, 88, 89, 121–123, 138–140, 147, Overfishing, 9, 483
149, 150, 196, 214, 233, 261, 262, 335, 342, 345, 348, 366, Overhangs, 71, 79, 219, 291, 292, 490
412, 413, 427, 448, 453–455, 486, 487 Overturning cells, 198
Octopuses, 292 Overturning circulation, vii, 96, 490, 507, 508, 510, 511
Offshore marine protected areas, 253, 254, 365 Oxcal 4.3.2 software, 68
Off-shore oil exploration, 537 Oxide(s)
Offspring, 335, 426, 430, 483, 484, 486, 489, 490 coatings, 97
Oil exposure, 448 patination, 20
Oil platforms, 393, 409, 494 Oxidise, 160, 438
Oil prospecting/prospection, 378, 384, 535 Oxygen
Old corallites, 394 concentration, 92, 235
Old specimens, 79 isotopes, 41
Oligochaeta, 318 Oxygen-poor, 48
Oligoelements, 453 Ozonation, 443
Oligo-Miocene, 500, 501
Oligotrophic, 78
Omnivorous, 513, 515 P
On board, 3, 4, 54, 96, 191, 257, 276, 436–442 Pacific Ocean, 10, 103, 234, 343, 344, 346, 418
On-land cold-water coral, 15, 68, 71, 79, 80 Packstones, 75, 324
Ontogenetic shifts, 488 Paddlewheels, 451, 458, 465
Ontogenetic vertical migration, 487 Palaeoceanographic, 41, 51, 60
Ontogenic, 461 Palaeoenvironmental setting, 93
Oocyte, 398, 399, 426, 429, 486 Palaeorelief, 86, 93
Oogenesis, 460 Paleoarchives, 5, 35, 41, 42, 61, 96
Opaque bands, 410 Paleoassemblages, 19, 51
Open access database, 67, 80 Paleobathymetric, 20
Open circuit, 438 Paleocanyon, 18
Open ocean, 20, 48, 49, 51, 438, 519, 542 Paleoceanographic, 41, 51, 61, 97, 406
Open sea eddy, 201 Paleoceanography, 23, 35, 100, 103
Open water system, 443, 445 Paleocliffs, 19
Operational models, 202 Paleoclimate
Operational Taxonomic Unit (OTUs), 379–382 archives, 95–105
Opportunistic, 318, 361, 363, 383, 384, 437 indicators, 405
feeding, 378, 392, 396, 459, 461 Paleoclimatic potential, 15
Optical resolution, 20 Paleoclimatology, 35
Oral-aboral axis, 399 Paleodepth, 18, 19
Oral pore, 461 Paleoecological reconstruction, 15–19, 24
Orbital-induced climate variation, 503 Paleoenvironment, 15, 18, 19, 23, 48, 49, 67, 80, 104
Oregon Institute of Marine Biology, 448, 449, 452 Paleoescarpment, 18, 76
Organic Carbon, 313, 398, 456, 459, 460 Paleontology, 24, 25, 80, 115
Organic matrix, 379, 406 PaleoPark, 93
staining method, 429 Paleo-phosphorus, 103
Organic matter (OM) Paleotemperature, 54, 502
fluxes, 7, 285, 396–398 Paleothermometers, 99–100
oxidation, 17 Pandalids, 320
Organic resources, 459 PANGEA, 204
Organic Rich Layer 1 (ORL1), 266, 267 Pan-Mediterranean, 196, 198
Organic waste, 443 circulation cell, 198
Orientation, 58, 62, 111, 147, 175, 177, 194, 258, 410 Paradigm, 47, 115–117, 483, 492, 514
Orpheus island, 384 Parameterization, 483, 495
Orthogonal, 410 Parameters, 7, 8, 10, 95, 96, 100, 103, 110, 111, 233, 274, 287, 366,
Ostracods, 23, 53, 319 373, 384, 392, 393, 397, 405, 411, 416, 417, 431, 442–444,
Other Effective area-based Conservation Measures 455, 463, 464, 466, 483–486, 489, 492, 493, 509, 517–520, 526
(OECMs), 540 Parasites, 452, 489, 514
Otolith microchemistry, 484 Parasitic, 316
Otranto Parasitism, 11, 346
Channel, 202, 236 Paratethyan, 48
Strait, 218, 236 Paratethys, 501–503
OTUs, see Operational Taxonomic Unit Parautochtonous, 19
Outcrops, 16–20, 22, 23, 25, 48, 73, 75–77, 79, 85, 86, 92, 93, 116, Parental colonies, 488
161, 162, 176, 203, 208, 245, 274, 276–279, 285, 286, 291, Parma, 75
292, 336, 338, 341, 350, 499, 501, 502 Parthenogenesis, 358, 398
574 Subject Index
Partial pressure, 518 Physicochemical, 5, 94, 100, 383, 392, 411

Particle advection, 285, 415 Physico-chemical properties, 5, 95, 96
Particle resuspension, 285, 415 Physiographic features, 159
Particle tracking algorithms, 485 Physiography, 36–37, 75
Particulate matter, 236, 451 Physiological functions, 229, 405, 439, 522–524
Particulate organic carbon (POC), 396, 456, 459 Physiological response, 53, 396, 436, 437, 440, 520, 525, 533
Particulate organic matter (POM), 237, 245, 285, 395, 396, 459 Physiological traits, 391
Passive continental margins, 501, 502 Physiology, 5, 7, 25, 95, 97, 99, 104, 363, 373, 383, 391, 392, 395,
Passive filter feeders, 456 399, 406, 435, 437, 440, 454–467, 510, 519
Passive filter-feeding organisms, 158 Phytodetrital food fall, 378
Passively-diffused particles, 484 Phytodetritus, 378, 398, 456
Past changes, 41, 95, 103, 104 Phytoplankton, 392, 453, 459
Past circulation, 502 Piedmont, 48, 74, 75
Pasteur pipette, 450–451 Pink colonies, 379
Patch(es), 32, 37, 97, 176, 193, 216–220, 228, 230, 233, 253, 265, Pink corals, 135, 228
267, 272, 286, 293, 319, 324, 340, 358, 359, 426, 539 Pink spiny lobster, 320
Patchy growth, 265 Pinnules, 125, 130, 138
Pathogens, 377, 378, 452 Pioneer, 3, 4, 22, 80, 96, 116, 221, 437, 475, 479
PCR, 387, 388 Piston coring, 22
Peak(s), 48, 135, 161, 228, 253, 281, 338, 379, 415, 489, 491 Pits, 336
height, 379 Planet, 150, 271, 477, 479
Pelagic larval duration (PLD), 365, 430, 483–490, 492–495 Planktivorous, 335, 349–350
Pelagic larval stage, 483 Plankton, 48, 192, 245, 340, 393, 452, 453, 488, 490, 536
Pelagic production, 396 Planktonic community, 298
Pelagic system, 245 Planktonic food, 396
Peloponnesus peninsula, 235 Planktonic foraminifera, 161
Pelops, 201 Planktonic foraminifer record, 23
Peloritani chain, 20 Planktonic larvae, 483, 486, 495
Pennatulacea, 6, 121, 122, 129, 138, 140, 143–147, 214, 233–235, Planktotrophic, 340, 399
427, 541 Planulae, 8, 9, 426, 429, 461, 484, 485, 487–492
Pennatulacean, 138, 143, 145–147, 149, 214, 233–235, 237, 259, 315, Plastic grid boxes, 438
513, 515 Plasticity, 80, 137, 139, 373, 382, 415
Pen shells, 336 Plastic sedimentary rocks, 261
Peri-Mediterranean region, 51, 68, 75–77 Plateau, 163, 236, 342, 380–383, 387, 388
Peristaltic pumps, 458, 465 Plate convergence, 501
Persian Gulf, 490 Platyhelminthes, 327
pH, 95–97, 100–104, 363, 374, 377, 391, 395, 396, 399, 416–418, Pleistocene
440, 443, 444, 447, 450, 452, 462–464, 518, 520, 524, 526, Challenger Mound, 17
531–533, 536 limestones, 19, 116
Phaceloid colonies, 135 mass, 163
Phenol-chloroform, 387 Pleistocene-Holocene boundary, 51, 54, 78, 79
Phenotypic plasticity, 80 Plexiglas, 443, 462
Phoronids, 18 Pliocene, 16, 23, 41, 47–49, 67, 75, 77, 79, 150, 213, 417
Phosphacline, 204 Plio-Pleistocene, 48, 214, 499, 502, 503
Phosphate concentration, 103 communities, 502, 503
Phospholipid-derived fatty acids (PLFAs), 459 Plio-Quaternary, 47, 163
Photic layer, 399 Pockmarks, 262, 266, 541
Photic zone, 462, 488, 535 POEM cruises, 201
Photographic, 4, 9, 111, 191, 192, 345 Pola, 4, 32, 226
samples, 192 Polar areas, 474
Photography, 162, 173, 177, 287 Policy makers, 11, 478, 479
Photo-lander, 340 Political communities, 159
Photo-mosaic, 178, 179, 184, 185 Pollutants, 274, 416, 452, 458
Photo stills, 157, 161 Pollution, 368, 378, 399, 513, 518, 526, 535, 536
Photosynthates, 393 events, 517
Photosynthesis, 387, 388, 467 Polycarbonates, 443, 450
Phototactic, 399 Polychaetes, 18, 19, 21, 22, 53, 162, 258, 259, 261, 263, 278, 295,
Phylogenetic, 123–125, 132, 140, 141, 145, 148, 366, 373, 374, 377, 296, 298, 316–318, 327, 340, 367, 399, 460
380–382 Polygons, 163, 164, 166
Phylogeny, 124, 132, 145, 373 Polymorphism, 123, 138, 359–363, 366, 367, 374, 379
Phylotype, 379, 382, 383, 388 Polynoidae, 318, 327
Physical damage, 291, 443 Polyp
Physical degradation, 537 activity, 394, 439
Physical environment, 397, 484, 486, 489 bail-out, 398
Physical processes, 483, 484 contraction, 393
Physical support, 536 retraction, 437
Subject Index 575
Polysaccharides, 406, 409 Protein(s)

Population skimming, 443
agglomerations, 508 turnover, 395
connectivity, 358, 398, 483–485, 489 Proteinase K-lysozyme, 387
density, 147, 426 Protein fractionators, 438, 450
dynamic, 10, 96, 194, 247, 424–426, 428, 430 PROTOMEDEA, 259
genetics, 132, 140, 238, 358–361, 363, 366, 373, 483, 493 Protozoan parasites, 452
sinks, 426, 430, 485 Provençal east, 196
sources, 426, 484, 485, 493 Provence coast, 22
structure, 249, 360, 373, 423–431, 493, 495 Provinces, 5, 6, 22, 31–33, 37, 40, 41, 57–59, 61–64, 75–77, 80, 92,
trend, 425 100, 110, 111, 157, 159, 163–165, 167, 178, 195, 207,
Porcupine Bank, 340 215–222, 224–230, 232, 234–237, 247, 253, 265, 266, 273,
Porcupine Seabight, 22, 41, 52, 77, 178, 340, 348, 410 286, 296–298, 312, 313, 319, 322, 324, 325, 337–341, 346,
Poriferans, 313–315, 327 347, 351, 406, 412, 418, 424
Porosity, 109, 111, 123, 463, 524 Proxy, 54, 95, 96, 98–101, 103, 104, 176, 235, 276, 279, 363, 398,
Porto Cesareo Marine Protected Area, 216 462, 486
Portofino promontory, 286 Pseudocolonial, 16, 221
Positively buoyant, 461, 488 Pseudo-colonies, 133, 272
Positive thermal ionisation mass spectrometry (PTIMS), 101 Pseudo-replication, 462
Post-Messinian, 16 Psychrospheric taxa, 52
Post-mortem, 17, 22, 97, 436 Public, 7, 11, 125, 449, 466–468, 473–478, 495, 535
Post-reproductive, 338 Punta Gamba di Donna, 19
Potentiometric titration, 464 Punta Mazza, 18
Pots, 346, 468, 541 Punta Milazzo, 19
Pourtalès plan, 123, 132, 134, 135 Push cores, 177
Precipitation, 17, 20, 36, 47, 51, 99, 101, 195, 200, 206, 411, 507, 509, Pyrosequencing, 377, 379–382
517–519, 536
efficiency, 99
Precompetency-period, 487–488 Q
Predation, 337, 346, 405, 416, 430, 486, 489 Quadrupole inductively coupled plasma mass spectrometry, 100
Predators, 325, 335, 340–342, 344, 345, 350, 399, 406, 454, 509 Quantitative, 18, 23–25, 102, 165, 167, 184, 233, 286, 336, 361, 431
Predatory pressure, 486 Quarantine aquaria, 443
Prediction, 11, 175, 197, 377, 396, 510 Quaternary
Predictive modelling, 291, 292, 540 CWC, 16, 68
Pre-industrial times, 391, 518, 520 sediments, 16
Pre-mixed gases, 440 Quick-maturing species, 486
Pressure, 102, 163, 173, 197, 204, 267, 437, 449, 511, 513, 518,
531, 540
ridges, 163 R
Prey Radial, 121, 132, 146, 147, 410, 412, 413, 490
capture, 392, 393, 397, 406 Radioactive dating, 413
diversity, 311 Radioactivity, 412
Primary productivity, viii, 54, 502 Radiocarbon, 68, 98, 117, 227
Primers, 366, 387, 388 dates, 117
Primosole, 18 Radiogenic isotopes, 95, 96, 413
Princess-Alice, 32 Radioisotope techniques, 411
Principle of Priority of the International Code of Zoological Radiometric
Nomenclature, 70 chronology, 23
Prismatic, 405 dating, 22, 54, 78, 79, 411, 413
Pristine, 16, 19, 23, 214, 233, 237, 427, 542 techniques, 68, 76
area, 237, 542 Radiometrically, 53, 97, 185
Probes, 103, 388, 464 Ramets, 359, 363, 454
Productive feeding, 335, 347 Ramified, 124, 133, 137, 142
Productivity, viii, 39, 41, 49, 54, 59, 76, 78, 80, 103, 262, 265–267, Random, 22, 359, 361, 366, 493
285, 368, 502 Randomly distributed, 92, 462
Profile, 37, 40, 175, 176, 181, 184, 201, 204, 205, 342, 357, 382, 412, Rapid accretion deposit (RAD), 373, 408, 409
455, 459, 463, 464, 488, 490 Rapid surface warming, 507, 509, 511
Profiling floats, 196, 202, 203 Rarity, 92, 164
Projections, 51, 426, 428, 429, 461, 511, 542 Real-time, 197
Prokaryotes, 327, 387, 388, 396, 440 Rear, 395, 397, 436, 437, 447, 452, 460, 461, 487
Prokaryotic community, 378 Recapture of larvae, 483
Proliferation, 57, 96, 267, 365, 444, 466 Recapture techniques, 413
Propagule, 8, 39, 357, 359, 485, 486, 490, 493, 513, 514 Recirculating pump(s), 438, 448, 450
Protaras, 257–259, 466 Recirculation flumes, 456, 457
Protect, 150, 165, 232, 253, 254, 263, 335, 368, 392, 405, 435, 473, Recolonisation, vii, 24, 79, 357, 361–363, 365, 366
535, 537, 539 Recombination, 358
576 Subject Index
Reconstructions, 5, 15–20, 24, 37, 78, 80, 86, 95–105, 110, 112, Resolution, 20, 24, 61–63, 95–97, 99, 104, 109–111, 158, 159, 173,
123–125, 132, 140, 184, 194, 197, 266, 358, 366 176, 184, 185, 196, 202, 214, 237, 274, 287, 361, 363, 366,
Records, 4, 5, 7, 15, 17–20, 22, 23, 31, 32, 42, 48, 51, 58, 59, 61, 67, 367, 384, 417, 425, 491, 492, 495, 503, 537, 540
68, 74, 85, 87, 96, 97, 99, 104, 116, 125, 126, 128, 131, 138, Resource, viii, 9, 80, 122, 150, 157, 159, 238, 251, 255, 272, 296, 335,
141, 143, 145, 147–150, 161, 185, 191, 199, 219, 228, 230, 337, 343, 358, 360, 393, 399, 424, 458, 459, 515, 535, 537, 542
246, 250, 259, 267, 274, 275, 278, 279, 281, 285, 313, 317, exploitation, 542
318, 324, 358, 360, 424, 509, 513, 515, 523 Respiration, 7, 206, 391–393, 395–397, 406, 440–442, 454–456, 458,
Recovery, 4, 19, 117, 150, 161, 168, 196, 232, 237, 251, 296, 351, 460, 462, 464, 517, 521–526
412, 417, 437, 467, 479, 483, 536, 538, 539 Response, 7, 10, 17, 23, 39–42, 53, 79, 115, 167, 184, 197, 235, 258,
capacity, 437, 536 312, 391, 393, 395–397, 399, 406, 411, 412, 415–417, 419,
Recreational fishing, 214 436, 437, 439, 440, 444, 455, 456, 462, 464, 474, 477, 519,
Recruit, 357, 423–425, 430, 485, 490, 491, 494, 533 520, 522–526, 531–533
Recruitment, 162, 219, 272, 286, 325, 393, 417, 425, 426, 429–430, Restratification season, 204
484–486, 488–490, 493, 494 Rhodes, vii, 17–19, 76, 85–90, 92, 93, 200–202, 204, 297, 490, 502,
positions of larvae, 493 514, 515
Recrystallization, 23 Gyre, 200–202, 204, 490
Recycling, 378, 393, 396, 438, 460 Rhone River delta, 491
Red coral, 7, 31, 140, 143, 253, 296, 315, 423, 425–428, 430, 441, 538 Ridge, 17, 57, 58, 61–64, 161, 165–167, 196, 220, 261, 265, 297, 340,
Red filters, 444 345, 500, 541
Red light bulbs, 444 Rifean corridors, 47, 48
Red Sea, 8, 15, 364, 418, 491, 500, 525 Rifting, 501, 502
Red shrimp, 232, 293, 312, 320 Rift zones, 502
Reef(s) Rigid species, 324
builders, 387, 391, 399 Rising sea level, 59, 267
initiation, 417 River damming, 507, 509
Reef-building, 265, 266, 360, 362, 363, 406, 436, 444, 489 River discharge, 8, 491, 518
Reflooding, 47–49 River freshwater discharge, 8, 507, 509
Refrigerators, 438, 439 River runoff, 36, 195, 507–509
Refuge, vii, 9, 136, 150, 250, 271, 285, 287, 320, 335, 337, 338, 340, RNA based clone library, 382
342, 344, 350, 351, 361, 366, 536 Robotic arm, 25, 177
Refugia, vii, 11, 61, 357, 366, 367, 491 Rockall Bank, 110, 341, 345, 349, 361, 368, 379–383, 387, 388, 541
Reggio Calabria, 18 Rocky outcrops, 161, 162, 245, 274, 276, 277, 285, 286, 291, 292,
Regional, 41, 60, 62, 75, 77, 200, 251, 266, 281, 296, 312, 357, 361, 336, 338, 341
363, 396, 419, 479, 499, 502, 510, 517, 518, 537–542 Rocky shoals, 247, 250, 347
Regional Fisheries Management Organizations (RFMO), 540, 541 Rodos Island, 514
Region Ocean Model System (ROMS), 491 Roll-back process, 501, 502
Release sites, 493 Roman Republic, 424
Remineralization, 103, 398, 417 Ropes, 194, 279, 293, 347
patterns, 103 Rotifers, 451, 453
Remotely operated vehicle (ROV), 4, 22, 23, 25, 115–117, 131, 157, Roughness, 37, 158, 176
159, 160, 162–164, 168, 177–180, 183–185, 191, 194, 216, ROV, see Remotely operated vehicle
237, 245, 249, 253, 257–259, 267, 271–278, 280, 286, 287, RRS Discovery, 440
291–293, 297, 312, 317, 337, 340–343, 345, 358, 359, 377, Rudstones, 49, 70, 74, 75, 166, 167
437, 438, 442, 460 Rugosity, 158, 176, 177, 184, 457
Remote sensing, 173, 181, 184, 197 Runge–Kutta method, 492
Remote Sensing OBIA (RSOBIA), 178, 181 RV Merian, 257
Renewal network, 338 RV Meteor, 32, 96, 117, 328, 440, 441
Repeated measures, 520, 523 RV Minibex (COMEX), 191, 441
Replicates, 100, 359–360, 436, 446, 447, 452, 454, 458, 462, 464, RV Pelagia, 384, 389, 440
521–523, 525 RV Urania, 32, 112, 116, 238, 328, 441
Replication, 452, 462, 520, 521, 525
Repositories, 80, 117, 125
Reproduction, 3, 7, 10, 132, 140, 236, 325, 337, 338, 346, 347, 350, S
358–360, 363, 391, 392, 398–399, 406, 425, 435, 437, 449, Sabellariid worm reefs, 336
454, 458, 460, 461, 485–487, 493 Sacrifice, 411
Reproductive output, 425, 426, 429, 486 Salento area, 48
Reproductive rates, 425 Salento Peninsula, 49, 218
Reproductive seasonality, 398 Salinification, 507, 509
Reproductive status, 398 Salinity, vii, 5, 8, 18, 23, 41, 47–49, 96, 102, 141, 160, 183, 195,
Reproductive traits, 8, 10, 484 197–208, 266, 267, 274, 276, 286, 383, 416, 417, 442, 443,
Reserve, 426, 514 445, 462, 463, 484, 486, 490, 491, 495, 499, 501–503,
Residence time, 100, 519 507–511, 518–521, 525, 526
Residents, 173, 176, 281, 384 maximum, 357, 360
Resilience, 95, 103, 358, 396, 398, 405, 406, 418, 444, 460, 524, 526, Salt, 47, 200, 207, 209, 387, 448, 507–510
535, 536, 540, 542 budget, 508, 509
Resistance, 358, 396, 468, 503 Saltening, 519
Subject Index 577
Sampling, 10, 18, 23, 25, 77, 79, 97, 100, 103, 111, 116, 121, 149, Sea cucumber, 292, 322
150, 177, 181, 216, 226, 237, 266, 271, 273, 276, 278, 286, Seafloor mapping, 164
312, 313, 317, 318, 327, 351, 357–364, 366–368, 377–380, Seafloor mining, 537
388, 395, 430, 431, 436, 437, 441, 442, 463, 464, 483, 488, Seafloor morphologies, 182, 285
489, 519, 520, 531 Sea-level
gear, 359, 436, 442 fluctuations, 47
SAMS, see Scottish Association of Marine Science oscillations, 47
Sand filter, 452 Seamounts, viii, 20, 23, 32, 57–59, 148, 149, 158, 159, 162, 192, 196,
Sandy, 36, 39, 74, 75, 90, 91, 161, 163, 233, 258, 267, 292 205, 206, 218–221, 223, 228–230, 233, 234, 237, 245, 257,
deposits, 36, 74, 163 262, 272, 280, 312, 313, 336, 338, 341, 358, 366, 392, 417,
San Filippo, R., 16, 19, 20, 69, 297, 303, 311, 317, 324, 535 427, 489, 490, 515, 535, 537, 539–541
Sant’Agata Fossili, 48, 74 east of Ibiza, 338
Santa Maria de Leuca (SML), 62, 76, 77, 117, 157, 159, 163–165, Sea of Marmara, 147, 246, 297, 500–501, 503
167, 273, 296–314, 319, 320, 323–325, 337–339, 346, 347, 351 Sea pens, 129, 140, 143, 144, 147, 149, 161, 213, 216, 219, 233, 234,
Pantelleria Island, 62 261, 262, 345, 349, 365, 445, 450, 453, 486, 541
Sant Sebastià, 291–293 Seasonally, 274, 487, 489
Sapropel layer, 266, 267 Seasonal spawning, 378
Sapropel S1 event, 98, 99, 165 Seasons, 10, 204, 393, 437, 438, 460, 461, 487, 489, 519
Sardinia, 4, 17, 21, 32, 37, 75, 98, 196, 207, 215, 216, 218–220, 224, Sea temperature, 374, 438
226, 228, 230, 232, 236, 247, 254, 286, 297, 306, 322, 338, Sea urchins, 217, 258, 292, 322
339, 347, 500–502, 542 Seawater cut-off, 444
Channel, 17, 21, 98, 216, 224, 228, 236 Seawater phosphate, 103, 104
Sardinian canyons, 272 Seawater temperature, 23, 95–97, 99–101, 104, 235, 267, 363, 392,
Sardinian Eddies, 207, 490 394, 396, 398, 416, 417, 438, 439, 444–446, 518, 524
Sardinian waters, 427 Seco de los Olivos, 6, 159, 298, 539
Satellite altimetry, 197 Secondary builders, 317, 327
Satellite imagery, 495 Secondary structuring role, 315
Saturation level, 377, 424 Sediment(s)
Saturation state, 99, 103, 235, 409, 518, 519, 522, 523, 526 blocks, 163–165, 167
Scale, vii, 6, 9, 24, 35, 37, 41, 48, 51, 53, 59, 61, 64, 69, 70, 78, 79, cores, 22–23, 58, 78, 79, 95, 104, 109, 165
95, 97, 99, 103, 104, 110, 111, 123, 124, 140, 144, 158–160, drift mounds, 42
163–166, 168, 173, 174, 176–178, 182, 184, 191, 194, patterns, 37
204–207, 209, 214, 220, 221, 233, 237, 259, 278, 285, 292, pockets, 48, 363
293, 296, 318, 323, 327, 336, 337, 340, 341, 347, 357–359, supply, 23, 54, 57, 59, 61
361–363, 365–368, 383, 384, 391, 393, 406–410, 413, 415, Sedimentary cores, 9, 42, 109, 112
416, 418, 419, 425, 430, 442, 455, 462, 463, 483–485, Sedimentary deposits, 35, 115
488–490, 492, 493, 495, 499, 501–503, 542 Sedimentary habitats, 312, 340
Scaling up, 533 Sedimentation, 10, 32, 35, 39, 96, 165, 219, 228, 235, 262, 272, 292,
Scanning electron microscope (SEM), 125, 142, 148, 328, 408–410 346, 396, 416, 417, 464
Scaphopod, 306, 318 Sedimentivorous, 322
Scars, 17, 18, 22, 346 Seepage, 261, 262, 265, 266
Scattered distribution, 265, 285 Seismic gap, 503
Scavengers, 335, 350 Seismicity, 503
Science-based management, 157 Self-recognition, 416
Scientific observers, 540 Self-recruitment, 426, 485, 493, 494
Scientists, vii, 4, 5, 11, 80, 116, 148, 150, 351, 373, 423, 424, 467, SEM, see Scanning electron microscope
473–475, 477–479 Semi-enclosed, 10, 35, 36, 214, 227, 419, 507, 531, 535
Scleractinia, 6, 15, 31, 51, 67, 75, 79, 121–123, 126, 127, 130–134, Semilithified matrix, 19
149, 253, 373, 374, 405, 538, 540, 541 Sensing platforms, 490
Scleractinians, vii, 5–7, 15–19, 21, 23, 25, 48, 52, 53, 68, 70, 74, 75, Sensitive habitats, 159, 336, 540
77, 80, 85, 92, 95, 97, 100, 102, 103, 115, 121–123, 126, Sensitivity
130–132, 135, 136, 140, 149, 150, 158, 163–165, 167, 196, analysis, 495
214, 229, 237, 253, 257, 261–263, 292, 296, 298, 314–316, to ocean acidification, 226
319, 320, 341–342, 347, 358, 363, 367, 373, 378, 384, 391, to temperature changes, 226
398, 399, 405, 406, 408, 411–414, 416–418, 427, 439, 444, Sensitization, 474, 477
445, 447, 448, 450–451, 454, 455, 458, 473, 485, 486, Sensory zones, 493
517–526, 535, 536 Septa, 75, 103, 123, 131–135, 410
Sclerites, 122–124, 138, 139, 141–144, 146, 147, 345 Serpulidae, 304, 317, 318, 327
Sclerochemical, 411 Serpulids, 16, 17, 19–24, 76, 79, 258, 296–298, 304, 317, 318, 327
Sclerochronological, 411, 455 Serranids, 325, 335, 350
Sclerochronology, 412 Serravallian, 49, 69, 74
Sclerodermite, 409, 410 Serravallian-Tortonian, 48, 49
Scorpaenids, 325, 344 Services, 15, 202, 203, 207, 208, 296, 424, 513, 514, 535, 537
Scottish Association of Marine Science (SAMS), 437, 440 Sessile, 36, 39, 61, 136, 141, 143, 147, 192, 195, 214, 221, 250, 253,
Scottish waters, 395 261, 262, 267, 298, 311, 320, 426, 456, 474, 484, 485
SDGs, see Sustainable Development Goals cnidarians, 214, 261
Seabed morphology, 62, 158 Seston, 254, 427
578 Subject Index
Settlement, 7, 36, 74, 173, 221, 235, 237, 261–263, 266, 267, 286, Skeletonised, 16, 22, 52, 111
298, 324, 399, 416, 417, 429, 465, 486, 493 Skimmer, 439, 448, 450
sites, 493 Slab, 161, 261, 262, 500–503
Sex ratio, 429 segments, 501, 503
Sexually, 358, 398, 454, 484 Slope, 32, 37, 63, 76, 85, 103, 122, 131, 143, 158, 161, 162, 165,
Shaking plate, 441 174–178, 180, 182, 185, 193, 207, 217, 219, 221, 232,
Shallow water–deep basin model, 47 234–237, 245, 247, 249, 257, 258, 274, 276, 277, 281,
Sharks, 160, 232, 337–339, 341, 342, 345, 350, 509 285–287, 293, 298, 313, 324, 337, 338, 341, 342, 344–347,
Shelf break, 122, 191, 219, 249, 322, 514, 535, 536 365, 383, 384, 453, 489, 501, 502, 513–515
Shelf edge environments, 246 sediments, 298
Shelf-incising canyons, 285 Slope-stability, 35
Shelf-slope exchange, 285 Sloping rocky outcrops, 291
Shells, 22, 111, 141, 161, 315, 322, 336, 399, 405, 408, 488, 500, 518 Slow growth rates, 97, 228, 232, 247, 251, 394, 415, 536, 539
Shelter, 7, 8, 121, 245, 272, 277, 285–288, 298, 311, 320, 325, Slow population dynamics, 247
335–351, 535 Small patch(es), 37, 219, 286, 324
Ship, 226, 437, 439 drifts, 37
Ship-board maintenance, 438 Small-scale contourite facies, 35–36
Shipping, 513 Smothering, 464, 465, 536
Shoals, 131, 215, 222–224, 229, 232, 247, 250, 347 Society, 3, 7, 11, 467, 473–479
Short-term, 47, 395, 397, 406, 412, 437, 439, 440, 462, 517, 520, 524 Soft bodied species, 122
Shuttle Radar Topography Mapping (SRTM), 287 Soft bottom, 18, 52, 74–77, 121, 125, 130, 135, 136, 138, 141, 149,
Sicié canyon, 192, 193, 311 200, 213–215, 219, 221, 232–235, 237, 258, 261, 262, 267,
Sicié submarine canyon, 186 277, 296, 298, 311, 312, 315, 318, 320, 347, 466, 539, 541
Sicilian Channel, 32, 306 Soft corals, 138, 159, 162, 213, 261, 344, 345, 410, 413, 445, 453,
Sicilian Stage, 16 536, 539, 541
Sicily Soft sediment induration, 39
Channel, 62, 195, 198–203, 206, 207, 216, 218–219, 224, 226, Soft substrate, 74, 535
228, 230, 232, 235, 236, 249, 253, 273, 279, 490, 502 Soft tissues, 132, 393, 405, 407, 467
Strait, 77, 323, 509 Sokastro islet, 19
Siculo-Tunisian Strait, 105 Solenogastre, 319
Side-effects, 411 Solid waste, 165, 346, 536
Sidescan sonar (SSS), 157, 159, 163–167, 176, 178, 184, 519 Solitary corals, 18, 24, 31, 70, 74, 93, 135, 166, 220, 221, 259, 278,
Sideways bottom current flow, 39 280, 363, 373, 393, 418, 533
Siena Basin (SB), 75, 302 Somatic mutations, 358
Siliciclastic, 71, 75 Sonne, 32
Siliciclastic-dominated Facies (SF), 75, 76 Source population, 426, 485, 493
Silicone tube, 454 Source-sink, 483, 493
Silt-clay deposits, 73 Southern Adriatic, 17, 32, 41, 42, 173–176, 199, 201, 202, 216–218,
Silting, 19, 36, 41 236, 272, 279, 297, 320, 324, 337, 338, 347, 365
Simulation, 197, 200, 202, 207, 413, 447, 484, 492, 493, 509, 519, Southern California, 344
536 Southern Chile, 346, 349
Sink, 198, 199, 405, 426, 430, 483–486, 493, 494, 518, 519 Southern Ocean, 96, 103, 413, 414
population, 426, 430 South Sardinia, 32, 33, 37, 41, 216, 218, 219, 224, 226, 236, 247, 297
Sipunculans, 318 South Tyrrhenian Sea, 219, 338, 347
Siracusa, 18 South-western Adriatic Sea, 542
Sites of Community Importance (SCI), 160, 251, 365, 539 South-western coasts of Sardinia, 338
Sites of conservation interest, 254, 535, 538, 539 Spain, 48, 74, 75, 124, 130, 131, 140, 145, 147, 149, 150, 207, 251,
Size, 8, 19, 22, 37, 38, 41, 62, 74, 75, 77, 97, 101, 110, 111, 125, 130, 365, 396, 428, 438, 439, 445, 449–450, 490, 539
131, 135, 137–141, 146–148, 159, 164, 166, 184, 216, 231, SPAMIs, see Specially Protected Areas of Mediterranean Importance
234, 274, 276, 311, 312, 317, 319, 324, 325, 327, 336, 337, Spanish margin, 265
342, 344, 345, 351, 357, 359, 360, 362, 364, 366, 369, 378, Spanish-Moroccan field, 57, 265
391, 392, 399, 409, 417, 424, 425, 428–431, 442–445, 450, Spatial
451, 454–456, 461, 462, 466, 467, 475, 486, 493, 495, 500, autocorrelation, 162
503, 522, 523, 525, 533 comparisons, 191
Skagerrak, 440, 441, 447, 462, 488, 521 coverage, 178, 540
Skate, 339, 344, 345, 350 heterogeneity, 245
Skeletal banding, 104 resolution, 111, 158, 159, 184, 185, 202, 417, 491
Skeletal extension, 519 Spatio-temporal distribution, 15, 67–80
Skeletal fusion, 416 Spawning
Skeletal growth, 100, 393, 405–408, 410–412, 419, 441, 455, 459, habitat, 337
465, 531 substratum, 232
Skeletal mass, 392 Special Areas of Conservation, 160, 254, 538
Skeletal microstructure, 17 Specialists, 192, 342, 350, 466, 474
Skeleton, vii, viii, 5, 7, 15–17, 20, 22, 23, 41, 52, 53, 67, 68, 75, 77, Specially Protected Areas and Biological Diversity, 537–539
78, 95–97, 99, 100, 102–104, 110, 111, 122, 123, 125, 131, Specially Protected Areas of Mediterranean Importance (SPAMIs),
132, 135, 137, 148, 221, 231, 249, 257, 258, 272, 298, 315, 164
322, 345, 363, 373, 378, 379, 393, 394, 398, 399, 405–413, Species richness, 32, 47, 121, 143, 147, 149, 161, 311, 313
416, 428, 444, 454, 455, 462, 465–467, 518, 524 Spectrophotometry, 464
Subject Index 579
Sperm, 398, 399, 461, 486 Subfossilised benthos, 20

Spermacysts, 398 Sub-grid scale processes, 492, 493
Sponge(s) Submarine banks, 158, 233, 272, 313
fields, 262, 336 Submarine canyon, 3, 4, 7, 9, 73, 85, 93, 135, 158, 191, 219, 271–281,
loop, 11, 396, 460 285–287, 291–293, 298, 312–315, 317, 320, 322–325, 406,
SRTM, see Shuttle Radar Topography Mapping 444, 474, 475, 490, 535, 536
Stable isotopes, 10, 393, 412, 458–460 walls, 535
Stagnant, 48 Submarine cliffs, 93, 427
Staining, 387, 393, 412 Submarine dune, 19
Stakeholders, 477–479, 542 Submarine landscape, 61–64, 158
Starvation, 393, 396, 398, 456, 524 Submarine lithification, 20, 22
Starved corals, 395, 398 Submerged coral deposits, 51
Static views, 196 Submergible surveys, 296
Stationary buoys, 495 Submesoscale vortices, 207
Statistical approaches, 158, 367 Sub-metrical resolutions, 158
Statistical models, 173 Sub-micron size, 409
Statistical robustness (SR), 517, 520, 521, 525 Sub-optimal conditions, 440
Stazzano, 74 Subpolar region, 509
Steady state, 197, 209, 425, 429, 508 Subpopulations, 357
Steady-state view, 197 Subsidence, 500, 501
Steep escarpments, 85, 92 Substrate, 15, 18–20, 22, 23, 25, 39, 42, 48, 74, 75, 85, 92, 116, 121,
Steep faults, 499, 503 125, 130, 136, 137, 139, 141, 143, 158, 161–163, 165, 175, 176,
Steep rough topography, 93 178–182, 184, 185, 191–193, 207, 214, 257–259, 261–263,
Steep slopes, 85, 185, 217, 287 265–267, 272, 277, 286, 291, 298, 315, 317, 318, 320, 323, 324,
Steep terrains, 285 327, 336, 337, 342, 345–347, 349, 351, 363, 398, 399, 407, 430,
Stem, 124, 125, 130, 316, 412 441, 449, 453, 459, 462, 477, 487, 493, 502, 535
Stenoecious, 213 Sub-surface layer, 202
Stenothermic, 51, 53, 78, 79 Subtropical gyre, 509
Stepping-stone, 485 Successful recruitment, 486
Stirone River chemoherm, 75 Suez Canal, 10, 513, 514
Stirrer, 440, 441 Sugars, 395
Stochasticity, 493 Suitability models, 173, 176, 181–183, 185, 207
Stoechades Canyon, 22, 192 Suitable habitat congruity, 484
Stoichiometric, 411 Sula Ridge complex, 17, 340
Stoloniferan, 139, 143, 315, 327 Sulphide deposits, 537
Stony corals, 131, 159, 179, 214, 216, 218, 221, 388, 412, 538, Sulphur compounds, 379
540, 541 Summits, 157, 163, 165, 196, 267
Stony reef-forming corals, 253 Sump filtration system, 466
Storms, 35, 207, 258, 274, 291, 293, 398, 454 Supervised, 6, 157, 158, 163, 165–167, 181, 182, 185
St Paul’s Bay limestone, 19 Supply of seawater, 437
Strait of Gibraltar, vii, 32, 36, 48, 142, 198, 209, 247, 273, 279, 287, Suprabenthic, 296, 319
295, 297, 298, 311, 317, 323, 324, 327, 365, 501, 503, 507, 519 Surface drifting platforms, 197
Strait of Sicily, 17, 21, 24, 41, 42, 100, 110, 111, 117, 143, 295, 297, Surface growth rates, 411
311, 315, 364, 365, 515, 542 Surface productivity, viii, 265, 267, 285
Stratification, 161, 197, 208, 253, 418, 490, 536 Surface tension, 461
Stratigraphic, 47, 48, 60, 61, 73 Surface waters, 36, 98, 103, 162, 200, 266, 267, 398, 415, 462, 487,
Stratigraphy, 22, 184 488, 490, 491, 493, 495, 507, 508
Stream, 438, 443, 490 Suroit, 32
Stress Survival rates, 425, 438, 489
period, 382 Suspended sediment, 40, 61, 262, 292, 293, 397, 443, 465, 536
response, 464, 520 Sustainable Development Goals (SDGs), 537
Stressors, 10, 185, 374, 395, 416, 417, 462, 485, 518, 525, 526, 533 Synergistic, 363, 368, 374, 395
Strict symbiont, 318 Synonymies, 31, 131
Strong currents, 148, 350, 392, 454 Synthetic simulation, 484
Strontium fluctuations, 410 Systematics, 6, 8, 80, 101, 122–123, 125, 131, 137, 145, 148, 150,
Strontium isotopes, 48, 100 167, 192, 196, 274, 291, 373, 387, 423
Structural species, 122, 245 Systemic errors, 495
Structuring, 6, 121, 137, 227, 249, 250, 293, 315, 365, 384, 483,
489, 538
species, 137, 227, 249, 293, 538 T
St. Vito Promontory, 322 Tank, 438–441, 444–452, 462–464, 466, 467, 521, 525
Subaerial outcrop, 18, 23 Taphocoenoses, 21, 318, 319
Sub-Antarctic, 97 Taphonomic, 9, 17, 18, 20, 22, 23, 73, 109, 110
Subaqueous evaporate, 47 Taphonomy, 15, 17
Subbasin, 202, 507, 510 Tasyo fields, 265
Sub-bottom profiles (SBP), 176, 181, 184 Taxa, viii, 8, 21, 31, 52, 53, 68, 73–75, 80, 115, 122, 123, 125,
Subfossil, 20–23, 31, 96, 116, 134, 161, 235, 296, 297, 317, 319, 130–132, 149, 150, 185, 191, 213, 214, 253, 298, 311, 312,
320, 322 317, 318, 320, 323, 327, 365, 366, 417, 513, 536, 538, 540, 541
580 Subject Index
Taxonomical expertise, 317 Tidal influence, 416

Taxonomy, 6, 24, 25, 70, 80, 121–151, 185, 192, 219, 237, 373 Tides, 35, 287, 392, 415
TDW, see Tyrrhenian Dense Water Time of spawning, 486–487, 489
Tearing, 502 Tisler Reef, 99, 396, 447
Technical diving, 245 Tissue
Technological developments, 4, 7, 173, 245 condition, 439
Technology(ies), 9, 16, 25, 117, 121, 168, 173, 185, 214, 221, 232, injuries, 437
378, 391, 423, 436, 438, 473, 477, 479, 492, 519 sloughing, 439
Tectonic(s) Titanium heaters, 462
evolution, 51, 499–504 Tjärno Marine Lab, 436, 456
hydrodynamics, 61, 64 TMF7, 379
processes, 261, 499, 501–503 Tolerant, 53, 60, 440
Tectonically-driven, 47, 64 Top-down approaches, 158, 174, 180–181, 184
Telegraph cable, 32, 393 Topographic highs, 57, 85, 92, 176, 207
Teleost fish, 194, 338, 347–350 Topography, 6, 20–22, 25, 57, 93, 162, 167, 184, 213, 221, 232, 237,
Teleosts, 194, 325, 338, 347–350 261, 262, 287, 291, 341, 347, 349, 413, 490, 535
Temperate corals, 99, 102, 399, 419, 426 Top predators, 509
Temperate zooxanthellate corals, 96 Tortona, 74
Temperature Tortonian, 48, 69, 74, 501
anomalies, 444 Total alkalinity, 394, 411, 444, 448, 455, 463, 519
controlled room, 443, 445, 448, 462, 463 Total Nitrogen (TN), 204
Temperature-dependent coefficient of respiration (Q10), 524 Total organic carbon (TOC), 204, 397, 398, 442, 521
Temperature-sensitive proxies, 99 Total Phosphorous (TP), 204
Temple University, 448, 449 Towed cameras, 4, 337, 346
Temporal comparisons, 192 Towed dredges, 165
Temporal resolution, 425, 491, 492, 495 Toxic chemicals, 345
Temporary extinction, 92, 165, 368, 417 Trace(s), vii, 17, 19, 23, 41, 95–98, 104, 148, 346, 374, 406, 459
Tenericutes OTUs, 380 elements, 95–97, 104, 374
Tentacles, 123, 124, 137, 138, 141, 142, 144, 146–148, 392, 407, 451, metals, 406, 412
453, 465 Tracks, 41, 98, 162, 163, 178–180, 191–194, 202, 204, 368, 424, 461,
Termofourà Formation, 73 485, 492, 537
Terrain Attribute Selection for Spatial Ecology (TASSE), 175–177 Tradeoff, 426, 492
Terrain morphology, 291, 292 Trajectories, 39, 42, 359, 492, 493
Terrigenous, 39 Trammel net, 245, 247, 536
Tethys Oceans, 500, 501 Transcriptomes, 123, 124, 140, 366, 367
Textural analysis, 166, 182 Transects, 61, 160, 164, 191, 274–277, 291, 344, 347, 361, 410
Thanatocoenoses, 319 Transfer, 7, 11, 202, 367, 407, 412, 425, 426, 430, 437–439, 461, 466,
Thanatofacies, 22, 296, 318 473–479, 493, 513
Thassos Island, 32, 279 Transient, 197, 199, 213, 342, 384, 406, 502, 508, 510
Thaumarchaeota, 388 Transition matrices, 425, 426, 430, 493, 494
Theca, 148, 410 Transplantation, 395
Thermal acclimatisation, 394 Transponder, 191
Thermal capacity, 518 Transport, 8, 35, 40, 165, 200, 202, 207, 221, 235, 281, 285, 293, 357,
Thermal constrains, 54 418, 426, 430, 436–439, 454, 456, 458, 485, 488, 492, 513
Thermal range, 53, 394, 396, 398 Transverse lineations, 163
Thermal shocks, 437 Traps, 22, 207, 346, 349, 384
Thermocline, 272, 398 Trawl fisheries, 514
Thermodynamics, 406, 509 Trawl fishing, 214, 226, 232, 234, 346
Thermohaline, 96, 199, 204, 490, 507, 508, 519 Trawling
circulation, 195, 507–510, 519 activity, 263, 291, 346, 351
Thermo-insulated bio-box, 438 marks, 191
Thermometer, 95 stress, 398
Thermo-regulated rooms, 444 Trawl surveys, 32, 253
Thermostad, 200 Treatments, 80, 192–194, 276, 387, 396, 412, 436, 447, 458, 462–464,
Thickening deposits (TD), 97, 373, 409–410 466, 467, 520–523, 532, 533
Thickets, 340, 359 Tree-like, 124, 125, 138, 139, 142, 247, 407
Threat, 9–10, 214, 259, 285, 291, 346, 377, 378, 391, 392, 405, T-RFLP, 379, 384
417, 418, 444, 474–476, 478, 479, 513–515, 531, 533, analysis, 379
536–538, 540 Tricase, 218, 225, 286, 287, 297, 339
Threaten, 51, 117, 164, 185, 214, 251, 298, 384, 391, 423, 515, 531, Triggering factors, 51
535, 537, 538 Trondheimsfjord, 379, 380
Three-dimensional frameworks, 245 Trondhjem Biological Station, 436
Three dimensionally complex habitats, 312 Trophic-carrying, 213
Threshold, 41, 111, 281, 394, 395, 424, 520, 522, 526, 540, 541 Trophic structure, 18, 396, 398
Tidal cycle, 158, 488 Trophic webs, 296, 313, 533
Subject Index 581
Tropical Uranium, 95
Atlantic, 74, 75 US eastern Atlantic margin, 22
corals, 96, 102, 103, 271, 373, 377–379, 382, 383, 387, 388, 392, U-series dating, 95, 117
393, 395, 396, 398, 406, 407, 409, 410, 427, 519, 525 UV steriliser, 443, 447, 448
environments, 100
region, 391
species, 373, 392, 419, 426, 486 V
True Mean Life, 98 Vagile fauna, 233, 250
Tsunamis, 35, 168 Valdivia, 32, 541
Tunisia, 514 Valle Ceppi, 73, 74
Turbidite facies, 36 Valle Palione, 18
Turbidity, 20, 160, 162, 536 Vallone Catrica, 19
Turbulence, 202, 206, 207, 451, 460, 461 Val Vergnana, 74
Turbulent, 35–42, 61, 207, 236, 237, 443, 458 Valves, 24, 449, 464
flow, 458 Var canyon, 234, 297
Turin Hills, 48, 49, 73 Variability, 42, 62, 74, 80, 96, 97, 99, 104, 131, 139, 148, 157, 159,
Turkey, 196, 513–515 166, 192, 197, 199, 201, 202, 204, 206, 267, 342, 367, 374,
Turnover, 17, 20, 23, 197, 395, 443 377, 382–384, 396, 398, 411, 413, 454, 492, 509, 510, 519,
timescale, 197 531–533
Tuscan Archipelago, 17, 22, 176, 223, 338, 347 Var submarine canyon, 286
TV-equipped devices, 22 Vaucluse, 75
Twilight zone, 387 Vector, 175, 176, 373, 475, 513, 542
Types or neotypes, 125 Vegetative reproduction, 454
Tyrrhenian basin, 229, 236 Velocity, 37, 38, 41, 42, 183, 207, 262, 281, 392, 443, 456–458, 465,
Tyrrhenian coral mounds, 508 488, 492, 500–502, 514
Tyrrhenian Dense Water (TDW), 207 Ventilation, 42, 47–49, 96–98, 104, 502
Tyrrhenian Sea, vii, 22, 31, 32, 62, 207, 219, 223, 226, 229, 230, age, 97
234–236, 261, 279, 312, 338, 347, 365, 427, 500–503 Vent site, 520
Tyrrheno, 31 Vercelli Seamount, 229
Verhulst, Pierre Francois, 424
Vertical migration, 261, 484, 485, 487–489
U profile, 488
Ultra-high resolution, 495 Vertical position, 488
Ultraviolet sterilisation, 443 Vertical reliefs, 336
Ultraviolet unit, 439, 450 Vertical stratification, 253
Unbranched, 124 Vertical topographies, 22
Uncultured bacterium clone, 379, 382 Vertical water flow, 488, 492
Underwater drop camera, 157 Vibrational frequency data, 101
Underwater forests, 427 Vicariance, 357
UNEP-MAP, 164, 537, 539 Video assisted technology, 438
UNEP/MAP/RAC-SPA, 254 Video footage, 9, 157, 160, 161, 173, 177, 192, 276, 341
Unique, 19, 67, 80, 97, 100, 103, 104, 136, 137, 142, 143, 147, 148, Videograb, 379
150, 221, 237, 257, 340, 342, 357, 359, 361–362, 408, 515, Video samples, 173
519, 535, 542 Video systems, 340
United Nations (UN), 537 Viral, 378
United Nations General Assembly (UNGA), 159, 537, 540 Visitors, 384
United States, 341, 342, 348, 349, 473, 475 Visual documentation, 477
University of Edinburgh, viii, 440, 447 Visual methods, 9, 191–194, 245
University of Gothenburg (UGOT), 436, 447–448, 451, 452, 458, 460, Vital effect, 95, 97, 98, 100, 103, 104, 412
461, 465, 468 Vital stages, 425
University of Oxford, 436 Vitamins, 453
University of Wageningen, 452 Viviparous, 345
Unlithified sediment, 18 VMEs, see Vulnerable Marine Ecosystems
Unsupervised, 158, 181, 185 Volcanic banks, 157, 159
Upper bathyal, 19, 48, 150, 249, 341, 363, 531 Volcanic bedrock, 161, 219
Upper Miocene, 49, 74, 143 Volcanic breccias, 161
Upper Pliocene, 23, 79 Volcanic edifice, 261
Upper slope, 76, 143, 162, 221, 245, 257, 324, 513–515 Volcanic islands, 218
Up-regulation, 102–104, 396, 418, 464, 522 Volcanic ridges, 57, 58, 162, 163
Upright position, 450, 454 Volcanic rocks, 74, 159, 161, 163
Upturned colonies, 258 Volcanoclastic, 39
Upward swimming, 461, 488 Volume scattering, 158
Upwelling, 185, 207, 237, 285, 490 Volumetric sampling, 18
Urania, 32, 112, 116, 238, 328, 441 Vugs, 19
Bank, 111, 219, 224, 297, 300 Vulnerability, 159, 164, 346, 518, 535, 536
582 Subject Index
Vulnerable, 11, 80, 137, 147, 157, 160, 165, 213, 214, 233, 234, 245, Western Mediterranean Transient (WMT), 208, 510
249, 251, 253, 254, 259, 262, 267, 281, 328, 341, 346, 347, West Melilla province, 58, 59
351, 357, 462, 483, 489, 518, 531, 538–540, 542 Whip-like, 124, 138, 142, 146, 234
deep marine ecosystems, 213, 509 White colonies, 379
species, 137, 234, 357, 483 White coral, 11, 16, 18, 19, 21, 32, 75, 85, 93, 115, 121, 125, 131,
Vulnerable marine ecosystems (VMEs), 11, 157, 159, 168, 233, 249, 135–137, 149, 213, 214, 218, 220, 221, 226–228, 237, 296,
251, 262, 280, 281, 347, 351, 538–542 319, 322, 324, 363, 439, 542
triad, 221, 363
White-coral biocoenosis, 296
W Wind farms, 360, 365
Wall microarchitecture, 75 Winds, 179, 199, 235, 369, 375
Wall of mouths theory, 489 World Wildlife Found (WWF), 122, 149, 475
Warming, vii, 9, 10, 51, 117, 378, 384, 391, 417, 418, 437, 440, 455, WoRMS, 11, 70
491, 507, 509–511, 514, 517–519, 525, 536 WoW, see Ways of the Waves
Warm shallow-water, 100
Warm water corals, 4, 383, 396
Washington, D.C, 32, 115, 349 X
Waste(s), 165, 192, 346, 391, 443, 448, 449, 452, 464, 466, 536 Xanthiids, 320
Water chemistry, 48, 97, 411, 451 X-ray Computed Tomography, 9, 109, 112
Water column properties, 158, 199 X-ray images, 109
Water exchange, 47–49, 411
Water flow regimes, 235
Water formation, 98, 105, 195–200, 207, 209, 507, 510 Y
Water-level sensor, 444 Yellow corals, 136, 214, 229, 230, 445
Water mass(es) Yield per recruit model, 424
exchange, 47, 48, 105, 197 Young corallites, 394, 524
tracers, 95, 98, 201, 202 Younger Dryas (YD), 53, 54, 58, 59, 67, 78, 266, 365, 508, 510
tracing, 97 Younger nubbins, 531
Water properties, 195–198, 449, 499 YouTube, 475
Water turbidity, 20
Wave maker pumps, 467
Wave regimes, 158 Z
Ways of the Waves (WoW), 475 Zagros suture zone, 500
Weak swimmers, 488 Zanclean, 47–49, 75
Weight(s), 183, 276, 278, 279, 347, 394, 411–412, 415, 454, 455, 465, Zanclean-Piacenzian deposits, 75
531, 540 Zealand region, 489, 518
Well-ventilated, 41, 49, 98, 99 Zoantharia, 6, 121–123, 127, 137, 149, 541
West Africa, 342 Zoantharians, 327, 513, 515
West Coast USA, 444, 473 Zoanthids, 127, 137, 139, 315, 316, 413, 447, 541
Western basin, 36, 54, 67, 78, 79, 115, 122, 131, 135, 138, 143, 147, ZOOlogical Data Exploitation system (ZOODEX), 191–194
149, 196, 197, 208, 228, 230, 234, 249, 360, 365, 509 Zooplankton, 325, 335, 340, 349, 378, 392, 393, 396, 398, 452,
Western Intermediate Water (WIW), 197, 199, 266 456, 459
Western Mediterranean circulation cell, 198 Zooxanthellae, 128, 393, 487
Western Mediterranean Deep Water (WMDW), 197–199, 207–209, Zooxanthellate, 71, 85, 96, 122, 393, 397, 464, 487
236, 508 Zygote, 359

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Coral Reefs of the World 9

More information about this series at http://www.springer.com/series/7539

ISSN 2213-719X ISSN 2213-7203 (electronic)

Library of Congress Control Number: 2018954937

© Springer International Publishing AG, part of Springer Nature 2019

Head Changing Oceans Research Group J. Murray Roberts

26 Occurrence of Living Cold-Water Corals at Large Depths Within

38 Cold-Water Coral in Aquaria: Advances and Challenges.

Species Index..................................................................................................................... 547

Subject Index..................................................................................................................... 555

© Springer International Publishing AG, part of Springer Nature 2019 3

1.3  editerranean Cold-Water Corals:

© Springer International Publishing AG, part of Springer Nature 2019 15

cristagalli), Caryophyllia spp., Javania eburnea (= J. cail-

Fig. 2.2 Examples of

Fig. 2.4 Hand samples

Fig. 2.5 Examples of CWC

Julian Evans, Leyla Knittweis, Joseph A. Borg,

Abstract The existence of cold-water corals (CWC), such as the

© Springer International Publishing AG, part of Springer Nature 2019 31

References Taviani M, Angeletti L, Antolini B, et al (2011) Geo-biology of

Abstract 4.1 Introduction

© Springer International Publishing AG, part of Springer Nature 2019 35

biogenic carbonate biogenic carbonate biogenic carbonate

Sandy mud with

Silty mud with

References Fink HG, Wienberg C, Hebbeln D, et al (2012) Oxygen control on

© Springer International Publishing AG, part of Springer Nature 2019 47

Abstract The Mediterranean is a marginal sea with limited communi-

© Springer International Publishing AG, part of Springer Nature 2019 51

Fig. 6.1 (a) Number of

Fig. 6.2 (a) Percentage of

common in the NE Atlantic, especially at lower temperature. References

© Springer International Publishing AG, part of Springer Nature 2019 57

© Springer International Publishing AG, part of Springer Nature 2019 61

Abstract boundary. “Golden ages” for the species Lophelia pertusa,

© Springer International Publishing AG, part of Springer Nature 2019 67

9.5  onclusive Remarks and Future

Abstract Twenty-seven scleractinian species, two of which zooxan-

© Springer International Publishing AG, part of Springer Nature 2019 85

0 10 20 30 650 700 750 800

from the island of Crete (1 outcrop; S. vermiformis; e.g., References

Abstract hand, these biologically-induced geochemical signals can

© Springer International Publishing AG, part of Springer Nature 2019 95

11.1 Introduction In recent years, an increasing number of studies involving

Fig. 11.2 (a) Mediterranean

Fig. 11.3 Coral Li/Mg vs.

Fig. 11.4 (a) Coral δ11B vs.

Fig. 11.5 P/Ca ratio

Lorenzo Angeletti, Matteo Bettuzzi, and Maria Pia Morigi

Abstract sawing is done at a frozen status, later de-freezing may, how-

Originally developed for medical diagnosis, CT application

© Springer International Publishing AG, part of Springer Nature 2019 109

Fig. 12.2 3-D reconstruction from Computed Tomography along core

et al. 2014). However, density measures obtained from CT

Fig. 12.3 Estimation of the

Conclusions Färber C, Titschack J, Schönberg CHL, et al (2016) Long-term macro-

Abstract 14.1 Introduction

© Springer International Publishing AG, part of Springer Nature 2019 121

Table 14.1 Mediterranean deep-sea corals

Head Changing Oceans Research Group J. Murray Roberts

26 Occurrence of Living Cold-Water Corals at Large Depths Within

38 Cold-Water Coral in Aquaria: Advances and Challenges.

Species Index..................................................................................................................... 547

Subject Index..................................................................................................................... 555

1.3 editerranean Cold-Water Corals:

Abstract 4.1 Introduction

9.5 onclusive Remarks and Future

11.1 Introduction In recent years, an increasing number of studies involving

Conclusions Färber C, Titschack J, Schönberg CHL, et al (2016) Long-term macro-

Abstract 14.1 Introduction

Cubozoa 14.3.1.1 Order Antipatharia

16.4.2.1 Automatic Classification 6.4.2.2 Habitat Suitability Models

Abstract 18.1 Introduction

19.4 Soft Bottom CWCs 19.4.1 Isidella elongata