Biological Sampling in the Deep Sea

Preface

The ocean covers 71% of the surface of the earth and the deep sea (considered here to be at depths greater than the continental shelf at 200–300 m) comprises the vast majority of this area. Seafloor habitats in the deep sea are many and varied, and include extensive areas of lower continental slope incised with canyons, beyond which there are large numbers of seamounts among plateaux, ridges, rises, plains and trenches, as well as hydrothermal vents and cold seeps. Until the late nineteenth century the depths beyond the photic zone were thought to be largely devoid of life. However, this concept has been disproven as scientific expeditions have discovered, and continue to find, a specialist deep-sea fauna that is among the most diverse on the planet.

Scientific knowledge of the deep sea has increased rapidly, but there exist large gaps in sampling coverage. As researchers have collectively worked towards increasing spatial coverage, inconsistencies have become apparent in how different habitats and regions have been sampled. Ultimately the extent to which data can be integrated will constrain how much our understanding of deep-sea ecosystems can develop. Furthermore, the pace of human impacts and changes in the deep sea are outstripping knowledge growth. There is growing pressure on deep-sea researchers to obtain data to understand the effects of fisheries and other human impacts that is vital for effective management and conservation.

In the wider scientific literature and online there already exist a number of publications and ‘grey literature’ reports discussing deep-sea sampling. In particular there are several methodological books (e.g. Eleftheriou & McIntyre, 2005; Eleftheriou, 2013; Danavaro, 2010) and general deep-sea texts (e.g. Gage & Tyler, 1991; Tyler, 2003). However, this book represents the first comprehensive compilation of deep-sea sampling methodologies for a range of habitats, and by dedicating a book specifically to deep-sea methods we are recognizing that the field of deep-sea research now warrants its own volume. The book fills a niche in the scientific and management communities, reviewing the real-life applications of current (and in some instances developing) deep-sea sampling tools and techniques across a range of deep-sea habitats and under a variety of conditions. In creating this book we have been able to draw upon the experiences of those at the ‘coal face’ of deep-sea sampling, expanding on the existing methodological texts while encompassing a level of detail often omitted from journal publications.

Ultimately we hope that the book will promote international consistency in sampling approaches and data collection, advance the integration of information into global databases, and facilitate improved data analyses and consequently uptake of science results for management and conservation of the deep sea.

Origin and scope of the book

The concept of this book was initially discussed by a small group of researchers comprising a ‘Standardization Working Group’ of the Census of Marine Life field project on seamounts (CenSeam). However, it rapidly became apparent that we could not, and should not, sample seamounts in isolation and the scope of the book was widened to encompass all deep-sea habitats.

The majority of sampling methods covered in the book target the mega- and macrofaunal assemblages associated with the deep seafloor. However, any study of the deep sea cannot exclude the wider influence of the entire water column and we also consider pelagic and environmental sampling. The main focus of the book by its very nature is biological sampling, but deep-sea research is a truly multidisciplinary venture. However, to encompass oceanographic and geological sampling in any detail would call for additional volumes that were beyond the realistic scope of our efforts. Nevertheless we hope all biologists can engage with other disciplines and encourage ongoing collaboration to obtain a wider understanding of deep-sea ecosystems.

In gathering authors to contribute to this book we have tried to cover as wide a range habitats and sampling equipment as possible. However, the content reflects personal experience and inevitably there will be omissions, but hopefully the book manages to build a solid foundation for future discussions of how to develop and progress biological sampling in the deep sea.

We hope that this book will appeal to a range of readers. Early career researchers can benefit from the experiences shared by those who have been on the trawl deck for many years, wisdom that is often not recorded in scientific papers and is often learnt the hard way. We also hope that the book will provide a scholarly platform and a solid foundation for students, as well as a valuable resource for environmental and science managers and policy-makers in detailing not only what tools are available to address issues in deep-sea management and conservation, but also in explaining some of the inherent challenges. The content of this book is based on the collective experiences of many deep-sea scientists, but we anticipate that even the most seasoned researcher will find this book of use. By documenting even the seemingly simplest of steps we might better identify where differences in approach occur, thereby providing opportunities for discussion and standardization across the research community to facilitate more robust data comparisons and analyses. Finally, the role of every research ship’s complement in making deep-sea research happen cannot be understated, and we hope that the book may find a place on board research vessels around the world as a reference to crews for the rationale behind some of the deployment strategies, and subsequent use of data.

The book cannot deal with every situation or gear type. Hence the chapters are cross-referenced and contain an extensive list of citations. The references included in the book are intended to give readers access to the main papers that can facilitate more detailed investigation of particular issues.

The book has been 5 years in the making, as the authors involved have tried to juggle the demands of their scientific work with the preparation of the various chapters. Research never stands still, and hence technological and sampling advances have occurred over that time period. We have tried to incorporate such changes wherever possible, and trust there are no major omissions that affect current ‘best practice’ advice or information.

Structure of Biological Sampling in the Deep Sea

The first part of the book sets the background scene with Chapters 1 and 2 considering general characteristics of deep-sea habitat and fauna, in the context of their influence on sampling methodologies. Chapter 3 moves towards the details of deep-sea sampling and discusses survey and sampling design. Recognizing that the motivations behind research surveys will vary, this book does not aim to be prescriptive, but rather to provide a toolbox of experience for users to utilize; with this in mind Chapter 3 draws heavily on case studies which bring to bear experiences from several research institutes.

Chapters 4–14 cover the major deep-sea sampling methods and equipment that are employed today. A ‘hands on’ description of the sampling operations includes information that is largely overlooked in the published literature. Each chapter encompasses a detailed description of the method, including information on gear specifications, modifications as well as notes on gear maintenance and handling; and also specific advice for application to different habitats and fauna. Treating sampling on the basis of gear type means there is some duplication and repetition, but this approach enables researchers to learn quickly about a particular gear type available to them, and keeps all relevant information together in concise sections. This structure emphasizes the need for consistency and comparability in the set-up and use of particular equipment, which is one of the priority objectives of the book. Chapter authors also detail what information must be captured for future cross-comparisons and analyses, as well as offering guidance on quality assurance. Sample sorting and processing is considered in the context of each method, and Chapter 15 includes a detailed discussion on the preservation and curation of biological samples.

However, important as ocean-going research and shipboard sampling are, ultimately they are only the beginning of the sequence of scientific research. Chapter 16 tackles what happens when ashore, and outlines best practices for developing and implementing deep-sea data management. Chapter 17 builds on this discussion to consider the peculiarities of deep-sea data analysis, with the authors drawing heavily on their own experiences and lessons learnt about data-poor situations and what to do and what not to do.

Scientific curiosity drove much of the early exploratory deep-sea research, but the current-day motivation to better understand this environment is now driven by an increasing need to manage and conserve deep-sea habitats and communities given a wide suite of anthropogenic threats. The knowledge base needed to effectively manage and conserve the deep sea is underpinned by good sampling design and practice, as well as effective transfer of information. Chapter 18 considers management approaches and outlines a process for developing biological sampling programmes in the deep sea that deliver both what scientists desire and managers or policy-makers need.

Ongoing technological advances drive continued exploration of the deep, and just as early researchers might never have anticipated the wealth of life that we now know exists, the deep sea is so poorly sampled we know there is a lot more to discover. Therefore the book ends with Chapter 19 considering how advances in technology and capability might drive further exploration, and what the future of deep-sea sampling might hold.

MALCOLM R. CLARK, MIREILLE CONSALVEY, AND ASHLEY A. ROWDEN

Acknowledgements

We thank the contributing chapter authors and many reviewers for their enthusiasm and efforts in bringing this book to fruition. CenSeam researchers are acknowledged for their role in developing the idea and concept, especially Alan Williams (CSIRO) for generating the original book proposal and helping launch the process. The contributions of other deep-sea Census of Marine Life projects are substantial, and we appreciate the willing involvement and commitment of ChEss, CeDAMAR, MAR-ECO and COMARGE. The book has taken 5 years to prepare and publish, and at times authors must have wondered if the idea and their efforts had slowly died. Their commitment to the process, and their acceptance of the delays and changes, are greatly appreciated.

Funding for much of this effort was from the Sloan Foundation, which was always supportive through the umbrella of the Census of Marine Life. The editors also received some funding for time from a NIWA research programme (Vulnerable Deep-Sea Communities, FRST contract CO1X0906).

We also express our thanks for the assistance of Wiley Blackwell’s publishing staff, especially Nigel Balmforth, Carys Williams, Kelvin Matthews, Harriet Stewart-Jones, Lea Abot, and Sandeep Kumar at SPi Global. The undertaking took much longer than originally anticipated, and their patience and understanding was greatly appreciated.

References

Danavaro, R. (ed.) (2010). Methods for the study of deep-sea sediments, their functioning and biodiversity. Boca Raton, FL: CRC Press.

Eleftheriou, A. (ed.) (2013). Methods for the study of marine benthos (4th edn). Oxford: Wiley Blackwell.

Eleftheriou, A., McIntyre, A. (eds) (2005). Methods for the study of marine benthos (3rd edn). Oxford: Blackwell Science.

Gage, J.D., Tyler, P.A. (1991). Deep-sea biology: a natural history of organisms at the deep-sea floor. Cambridge, UK: Cambridge University Press.

Tyler, P.A. (ed.) (2003). Ecosystems of the deep oceans. Amsterdam: Elsevier.

Chapter 1

Deep-Sea Benthic Habitats

Paul A. Tyler1, Maria Baker1 and Eva Ramirez-Llodra2, 3*

¹ National Oceanography Centre and, University of Southampton, Southampton, United Kingdom

² Institut de Ciències del Mar, Barcelona, Spain

³ Norwegian Institute for Water Research, Oslo, Norway

Abstract

The oceans were observed to be deep during the great age of exploration in the early to mid-nineteenth century. Subsequent exploration demonstrated that the ocean was bisected by underwater mountain ranges and dotted with abyssal hills. With the advent of the echosounder and latterly multichannel swath bathymetry, we now know that the deep ocean has topography as diverse as found on land. In the last 30 years, with an increase in deep-sea scientific activity and the use of underwater vehicles, we have learned that the deep sea consists of a series of habitats and ecosystems interconnected by hydrography and topography. The more recent challenges have been how to sample and analyse these separate habitats and ecosystems. This chapter describes the different environments and briefly outlines the main methods of sampling for each habitat or ecosystem. More detailed aspects of these sampling methods are found in subsequent chapters.

Keywords sampling, continental slope, canyon, cold-water coral reef, cold seep, mud volcano, mid-ocean ridge, hydrothermal vent, abyssal plain, trench, seamount

1.1 Introduction

Since the great age of oceanic exploration sailors have recognized that the oceans get deeper as their ships move away from the coast. The abruptness of this increase in depth was known to vary throughout the global ocean, with extensive shallow shelves off some coastlines, such as northwestern Europe, and precipitous increases in depth close to shore in other areas, as seen in the southeastern Pacific. In an age of cast lines to determine depth, data on oceanic depths was limited and accumulated slowly; it was only when there was a technology imperative, such as the seabed survey by HMS Cyclops in the North Atlantic prior to the laying of the first transatlantic telegraph cable in 1857, that our knowledge increased. This survey demonstrated that, on leaving Europe, the cable would cross the continental shelf, sink across the continental slope and cover most of its distance across the Atlantic on abyssal plains at depths greater than 5000 m (Murray & Hjort, 1912). However, the great depth of the Atlantic appeared to be bisected by a linear structure we now call the Mid-Atlantic Ridge that forms an element in a submarine mountain chain that circles the globe. These ‘primitive’ methods of sounding continued well into the twentieth century, so our knowledge of the ocean seafloor was composed of spot depths on naval charts.

The advent of the echosounder in the 1930s gave a continuous record of the depth of the seabed traversed, and increased the resolution of depth measurements considerably. It was the compilation of all the data to date in the early 1960s that gave rise to the iconic seafloor figure produced by Bruce Heezen and Marie Tharpe, which integrated for the first time depth measurements into a single three-dimensional figure. And what a figure this turned out to be. This and subsequent maps of the world’s seafloor revealed that the oceans were more complicated than simple deep basins covering ~70% of the surface of the Earth (Fig. 1.1). The most prominent features were apparently flat plains between 3 and 6 km depth that cover 50% of the surface of the Earth (Figs 1.1 and 1.2).

Fig. 1.1 Bathymetry of the global ocean showing a selection of the main features. MOR, mid-ocean ridge; AP, abyssal plain; TF, transform faults; MV, mud volcanoes.

Fig. 1.2 Hypsographic curve of the percentage of the global ocean at 1000 m depth intervals.

In many places, these plains were not only separated by submarine mountain ranges but were pockmarked by individual mountains or groups of mountains now termed seamounts. Particularly obvious in the Pacific was a series of very deep linear basins referred to as trenches, which are now known to occupy only 1% of the ocean but extend to the greatest depths of just short of 11 000 m. As we zoom in on the seabed topography, we see a steep slope between the shallow continental shelf and ocean basin referred to as the continental slope, the sediment-draped base being called the continental ‘rise’ or ‘fan’, although there is some dispute about this terminology. From the 1990s, widespread use of precise satellite navigation and a new generation of multibeam echosounders producing 3D swath images of the sea floor (Fig. 1.3) revealed further details. The continental slope may be smooth or bisected by submarine canyons that, at first glance, appear as gashes normal to the submarine contours. The continental slope is also a major site for cold seeps, one of the forms of chemosynthetically driven ecosystems now discovered, particularly in sedimentary areas. A similarly functional ecosystem is found along the mid-ocean ridges (MORs) and other volcanic areas, such as back-arc basins and subduction zones. Here, hydrothermal vents, so-termed owing to the expulsion of hot fluid, rich in sulfide, methane and dissolved minerals, support abundant local communities. Related faunal communities are found on even more localized habitats, such as whale falls and other organic inputs such as wood and kelp (at a scale of metres) that form their own ephemeral ecosystem on the seabed.

Fig. 1.3 Three-dimensional image of the Nazaré submarine canyon and nearby continental slope off the coast of Portugal showing the main features of the continental slope and a canyon. The view is to the east from open ocean.

It is the scale variation from thousands of kilometres on abyssal plains or along mid-ocean ridges to the small decimetre scale of vents and organic falls, together with the type of substratum, whether sedimentary, rock or biogenous, that drives the different sampling strategies employed to understand deep-sea ecosystems. It is only in the last 20 years or so that we have truly resolved the deep sea into its component ecosystems. Although available information is still limited and we do not know the exact extension of most of these ecosystems, deep-sea research has greatly developed in the last decades (Danovaro et al., 2015; Ramirez-Llodra et al., 2010a).

We will now describe the main features that will define sampling strategies for these different systems. Our approach is to examine the deep sea by moving out from the shore over the continental shelf and margin, out over the abyssal plains to reach the MOR systems and eventually the trenches or subduction zones. Embedded in these global scale features are smaller scale habitats such as cold-water coral reefs, canyons, seamounts, cold seeps and hydrothermal vents. We will define each habitat, examine the main sampling methodologies and discuss their limitations (Table 1.1).

Table 1.1 A summary of the main deep-sea habitats, their definitions, and the types of sampling methods, as well as the main considerations for each method

1.2 Ecosystem and habitat diversity in the deep sea

1.2.1 Moving into deep water

Although we now recognize different ecosystems and habitats within the deep sea, it is essential to acknowledge that they are all interlinked inter alia through hydrography in the water column, primary productivity arising from vertical flux of surface production or microbially mediated chemosynthesis and variation in the composition of the seabed from soft sediments to rocky outcrops.

As we move away from shore, the seabed sinks gently to a depth of 200 m. This is the continental shelf (Figs. 1.2 and 1.3) that provides most of the current ecosystem services from the ocean. In Antarctica the shelf occupy depths down to ~600 m as a result of the weight of the icecap on the surrounding continent. Throughout the world, the edge of the continental shelf is defined by an increase in the angle of the seabed (the shelf edge) (Fig. 1.3) and from this point down to depths of ~3000 m we find the continental slope (Figs 1.2 and 1.3). Together these are referred to as the continental margin and represent the most diverse collections of habitats in the ocean (Menot et al., 2010), including soft sediment slopes, canyons, cold seeps, cold-water corals and brine pools.

Continental slopes vary throughout the global ocean, mainly determined by whether they are passive or active margins. Bordering Europe, the eastern United States, eastern South America, all Africa and Australia, margins are passive and extend for thousands of kilometres. In many cases the continental slope increases in depth at an angle of about 8° (equivalent to the relatively gentle slope on a hillside). Although rock outcrops may be present, most of the slope is covered with sediment (Fig. 1.4a) and at the base of these slopes there is a decrease in the angle, giving rise to the continental deep-sea fan (or rise). In certain conditions where there has been a catastrophic influx of sediment into the deep sea by turbidity currents (Talling et al., 2007), there is the formation of a more specialized sedimentary feature called a turbidite. Along active margins, such as off the west coast of North and South America, the continental slope plunges straight down to the adjacent trench and has no obvious continental fan. The sedimentary environments of the continental slope and fan (especially on passive margins, although not turbidites) give rise to some of the highest biodiversity in the deep sea (Grassle & Maciolek, 1992). Since the nineteenth century, the traditional methods of sampling these areas have included trawls, sleds and box-corers, and these methods are still widely used today (Table 1.1), although they have been supplemented by the use of submersibles and remotely operated vehicles (ROVs) for small-scale work and autonomous underwater vehicles (AUVs) for wider scale surveys.

Fig. 1.4 (a) The continental slope seabed at 2200 m depth in the Northeast Atlantic showing ophiuroids on foraminifera ooze.

(Photograph by P.A. Tyler.)

(b) A drop stone in the continental slope at 2639 m in the Northeast Atlantic showing the winnowing of sediment downstream of the drop stone and current generated ripples in the background.

(Photograph by P.A. Tyler.)

(c) Bathymodiolus mauritanicus alive and dead on the Darwin mud volcano at 1100 m depth.

(Photograph courtesy of NOC/NERC. Reproduced with permission.)

(d) The frame-building cold-water coral Lophelia pertusa in the Whittard submarine canyon at 1300 m depth in the Northeast Atlantic.

(Photograph courtesy of NOC/NERC. Reproduced with permission.)

(e) The Porcupine Abyssal Plain at 4800 m in the Northeast Atlantic showing tracks, trails and pits in which phytodetritus can accumulate. The small holothurian is Amperima rosea.

(Photograph courtesy of DSM Billett NOC/NERC. Reproduced with permission.)

(f) Dense populations of the yeti crab Kiwa tyleri and the barnacle Vulcanolepas sp. at hydrothermal vents along the southern part of the East Scotia Ridge, Antarctica, 2500 m depth.

(Photograph by ChEsSo consortium.)

Not all margins follow this simple pattern and it is the heterogeneity of environments that leads to the apparent high species diversity found at these bathyal depths between 200 and 3000 m (Levin et al., 2010). Where the continental slope is steep enough to prevent settlement of sediment and bedrock forming, the margin is exposed (Tyler & Zibrowius, 1992). Hard substrata also occur at higher latitudes in all oceans where drop stones from melting icebergs, both past and present, increase the local heterogeneity of the seabed. Such drop stones interact with the local hydrography, modifying the sedimentology of the immediately adjacent seabed (Fig. 1.4b). In such a situation, sessile attached megafauna may be found, which are not easily sampled other than by the use of submersibles or ROVs (Tyler & Zibrowius, 1992). The ripples and winnowed sediment observed in Figure 1.4 are evidence of current flow along the contours of the continental slope.

Continental margins can also be impacted by oxygen-minimum zones (OMZs) (Levin, 2003). These zones occur at bathyal depths, particularly in the eastern Pacific and the Arabian Sea, where sinking organic matter from high surface production is remineralized, with heterotrophic bacteria stripping the water column of oxygen. Where the OMZs impinge on the continental slope, the fauna at the seabed tends to have reduced diversity, although some species are adapted to hypoxic conditions (Creasey et al., 1997). There is no special sampling strategy for OMZs, although sampling of the water column and interstitial salinity from sedimentary cores become important. The use of perspex cores in a megacore allows visual examination of the cores to show the various layers of change down the upper sedimentary column.

The apparent ‘smoothness’ of the continental slope is bisected in many areas of the global ocean by submarine canyons. These arise close to the shelf edge or part way across the shelf and form a deep chasm normal to the contours of the slope (Fig. 1.3). Canyons are subjected to specific geochemical, hydrographic and sedimentological processes (Canals et al., 2013) that enhance organic matter transport (Puig et al., 2003) and shape faunal community composition and structure (Ramirez-Llodra et al., 2010b; Schlacher et al., 2010). The formation of submarine canyons has led to much debate, whilst the environmental conditions within canyons such as strong currents and turbidity flows have hindered their study. Deployed equipment, such as current meters, can be swept away and lowered corers may be difficult to position where intended (Canals et al., 2006). Trawls are invariably lost, except in canyons where the topography is particularly well known. The most successful recent studies of canyons have employed ROVs (Huvenne et al., 2011), but still the use of such powered vehicles present challenges even in moderate currents with suspended sediments in canyons (Tyler et al., 2009). A second major problem for canyon analysis studies is the extreme heterogeneity (of depth, substratum type, seabed morphology, etc.) at different scales from thousands of kilometres down to metres where seabed type and depth may vary, whereas currents and suspended sediment load may vary on a tidal time scale.

Another feature of the continental margin are cold seeps (Sibuet & Olu-Le Roy, 2002; Levin, 2003). Cold seeps are environments where biogenic or thermogenic methane and biologically mediated hydrogen sulfide form the basis for primary production for the local food web (Tunnicliffe et al., 2003). The name of the environment derives from the seepage of these compounds in the sediment and that there is no increase in temperature (Levin, 2003). One of the most common forms of cold seep is the mud volcano, of which classic examples occur in the Gulf of Mexico, Barents Sea (Haakon Mosby Mud Volcano), Mediterranean Sea and the Gulf of Cadiz (Fig. 1.4c) (Olu-Le Roy et al., 2004; Vanreusel et al., 2008). Mud volcanoes look like the classic ‘cow pat’ and can be 100–200 m diameter. Infrequently mud pours out of the mud volcano and forms a slide down the flank of the volcano. Typical macrofauna include siboglinid tubeworms and bathymodiolid mussels (Fig. 1.4c) as found at hydrothermal vents. In addition, some mud volcanoes support colonies of octocorals, presumably feeding on the local bacterial production (Levin, 2005). On passive margins are found ‘pock marks’ (Ondréas et al., 2005; Olu-Le Roy et al., 2007). Pock marks are conical dips in the seabed sediment that often have associated seeps because of gas loss. In the Gulf of Mexico, a highly specialized form of cold seep is the ‘brine pool’ (MacDonald et al., 1990). This pool is some 30 m long and contains water at 120 ppt salinity. At the base of the pool is a salt dome and arising through the waters of the pool and the surrounding sediment is methane that fuels the methanogenic bacteria endosymbiotic with the mussel Bathymodiolus childressi. This mussel bed has a distinct fauna that contribute to the local diversity. Other small forms of cold seep are methane hydrates that appear to support an endemic species, the ice worm Hesiocaeca methanicola (MacDonald et al., 2003). Another highly specialized type of cold seep are the Campeche asphalt volcanoes found in the southwest Gulf of Mexico (MacDonald et al., 2004). These are unique habitats characterized by the episodic intrusions of semi-solid hydrocarbons that spread over and form structures with a significant vertical relief: the Chapapote knolls. Finally, one of the most recently discovered novel forms of seepage are the ‘hydrothermal seeps’. These hybrid systems, where methane seepage and diffuse hydrothermal flow are found together, have been documented along the Costa Rica margin (Levin et al., 2012).

Cold seeps, mud volcanoes, pock marks and other such features present their own sampling challenges. In most cases they are relatively small and, although sedimentary, they are not easily sampled by corer from surface ships. The most successful programmes for the analysis of cold seeps have involved the use of visual observation, faunal sampling and coring from submersibles and ROVs.

A final specialized environment of the continental margin is that of cold-water coral reefs (Freiwald, 2002). Most people are familiar with tropical shallow water reefs, the corals of which rely on symbiotic zooxanthellae for the deposition of calcium carbonate. Typically at bathyal depths in the ocean, there is a suite of corals that are azooxanthellate (having no zooxanthellae) but are successful in building reefs. The best known of these corals is Lophelia pertusa (Fig. 1.4d), but they also include the coral genera Oculina, Madrepora and Solenosmilia. These corals are ‘frame builders’, the frame being calcium deposited by the coral. The interstices of the frames provide a habitat for a wealth of invertebrate fauna and fish, making them an exceptionally high biodiverse environment. These reefs may be found throughout the global ocean but are particularly common in the North Atlantic (Zibrowius, 1985; Mortensen et al., 2008; Davies et al., 2008). They are especially vulnerable to deep-sea fishing where the corals are destroyed by the nets of heavy fishing gear that may clear an area of its corals and all the associated fauna (Hall-Spencer et al., 2002). Cold-water corals present difficulties for sampling in both practical and legal terms (e.g. some deep coral reefs are protected from disturbance and only non-destructive scientific sampling is allowed). Today, the main sampling effort is by the use of ROVs, but cold-water corals may also be surveyed by side-scan sonar, towed cameras and the use of AUVs.

1.2.2 The most extensive benthic environment on Earth

As we reach the bottom of the continental slope, the seabed starts to level off and between 3000 and 6000 m depth we have the most extensive benthic environment on Earth: the abyssal plains. These plains cover 50% of the total Earth surface (Fig. 1.2) and, although they vary depth and contain both basins and hills on a scale of kilometres, their slope is imperceptible. All the oceans of the globe have abyssal plains (Fig. 1.1). The original perception was that they were flat and featureless and, when viewed by low-resolution multibeam swath bathymetry from a surface vessel, this may appear to be the case. The traditional method for sampling the abyssal plains has been the use of trawls and sleds for larger fauna, box-corers for macrofauna, and multicores for meiofauna. Photography gives an in situ view of the seabed and it was soon realized that, although flat, there was considerable heterogeneity within this mainly sedimentary environment (Fig. 1.4e). Simply, there are bumps and dips often at the sub-metre scale. The bumps may be mounds formed by burrowing organisms living in the sediment and close examination shows that this disturbance affects the local biodiversity. Tracks and trails also create very small-scale disturbance that can lead to heterogeneity on the sub-metre scale. Dips in the seabed often get filled with phytodetritus from surface production, which has sunk to the seabed and collected in these hollows. In the Pacific, manganese nodules are scattered on the abyssal plain and form their own unique ‘province’, with the manganese nodules supporting a fauna composed mainly of foraminifera (Mullineaux, 1987; Miljutina et al., 2010). In the Mediterranean Sea, anoxic hypersaline pools have been found at abyssal depths (van der Wielen et al., 2005). Such environments were thought to be the preserve of microorganisms only, but Danovaro et al. (2010) have shown that at least three new species of the phylum Loricifera are capable of living under these conditions.

This habitat variation on the extensive abyssal plains leads to high diversity but low biomass amongst small infauna, including polychaetes, nematodes and peracarid crustaceans (Vanreusel et al., 1995; Lambshead et al., 2001; Brandt et al., 2007; Levin et al., 2010) although biomass is low as a result of low food availability (Smith et al., 2008). Thus the problem for sampling abyssal plains is that, by trawling over a couple of kilometres of seabed, the trawl will integrate the diversity of the seabed, whereas coring or sampling by submersible or ROV will differentiate the biodiversity on a micro-scale. Mosaicking from ROVs is developing as a tool to examine the sub-metre scale variation on abyssal plains.

Although extensive, the abyssal plains may be dotted, or even peppered as in the Pacific, by seamounts. There is a very specific definition that states seamounts are volcanoes, usually extinct, that rise hundreds or thousands of metres above the surrounding seafloor (Koslow, 2007; Pitcher et al., 2007) (Fig. 1.5). They are formed at MORs and are carried across the floor of the ocean by tectonic plate movement. This is seen particularly elegantly in the Emperor seamount chain formed by the Pacific hotspot that is now creating the Big Island of Hawaii. As these islands are moved to the northwest, they are eroded away to below sea level to form seamounts or guyots (where the top of the seamount is particularly flat, as in the Anton Dohrn seamount in the Northeast Atlantic (Fig. 1.5)). All seamounts are steep sided and their shape modifies the flow past them, with flow accelerating near the summit (Genin et al., 1986). Because of the steep sides and the accelerated flow over seamounts, the associated fauna is often sessile and filter feeding and includes a high abundance of all types of coral (Clark et al., 2010). Such an environment, as with cold-water coral reefs, attracts a high invertebrate and vertebrate diversity. This, together with the trapping of vertically migrating pelagic organisms, makes seamounts potentially intense fishing grounds and some seamounts in the global ocean have been devastated by deep-water fishing (Rogers, 1999; Althaus et al., 2009).

Fig. 1.5 Swath bathymetry of the Anton Dohrn seamount with its flat top, technically a guyot.

(Image courtesy of Colin Jacobs, NOC.)

An additional stress on seamounts is when the top of the seamount protrudes into the OMZ, which results in a natural reduction in biodiversity over the top of the seamount (Wishner et al., 1990). As with many of these specialized environments in the deep sea, traditional sampling methods have limitations, and submersible technology is often the preferred way of studying seamounts, although cameras towed from surface vessels have been used successfully (e.g. Rowden et al., 2010).

1.2.3 Mountain chains and hot fluid

The abyssal plains do not extend from continent to continent. As one moves across the ocean, there is a decrease in water depth, an increase in the ruggedness of the terrain and an increase in the proportion of rock at the seabed. This is the foothills of the MOR (Fig. 1.1), a 60 000-km-long structure that runs along all oceans. The MOR is the site of formation of new ocean floor. As the ocean plates are dragged down into the subduction zones, new seafloor material is added at the MORs. Mid-ocean is a bit of a misnomer, as these ‘spreading centres’ are roughly mid-ocean in the Atlantic and Indian oceans but are asymmetrically offset to the east in the Pacific (Fig. 1.1). The correct term should be spreading centres, but MOR is in common use. We know very little about the environment of MORs except for hydrothermal vents. The cross-section of the MOR can vary from a deep summit axial graben of 1000 m (as seen in the Atlantic) to the very shallow axial valley seen along the East Pacific Rise (Van Dover, 2000). More distinctive features of the MORs are the transform faults (Fig. 1.1) that appear as giant slits at right angles to the main axis of the ridge. These transform faults allow deep circulation between the deep basins either side of the MOR and may prove to be important conduits of reproductive propagules between the different ocean basins. Although of great linear extension, the MOR has not been sampled extensively, although the MAR-ECO and ECOMAR projects have examined the Mid-Atlantic Ridge close to the Charlie–Gibbs Fracture Zone (Bergstad et al., 2008). Remarkably, they were able to trawl areas of the ridge as well as using corers, submersibles and ROVs.

A distinctive feature of spreading centres are the hydrothermal vents. These were first discovered in 1977, when geophysicists could not explain the heat loss of the Earth’s interior by conductive heat loss alone, citing the expected presence of convective heat loss. Along the Galapagos Rift, they found the predicted convective heat loss and serendipitously discovered what became known as the hydrothermal vent fauna (Corliss et al., 1979). A hydrothermal vent occurs when seawater has percolated through the oceanic crust, reacted with the subsurface rock, been heated by magma and had its chemical composition changed by removing all oxygen and magnesium, reducing sulfate to sulfide and incorporating metals. The water released at the hydrothermal vent is rich in hydrogen sulfide, which reacts with seawater to precipitate as sulfide (Van Dover, 2000; Tolstoy et al., 2008). The formation of the chimney from which hydrothermal fluid emanates varies in structure and may affect the distribution of local fauna. In the Northeast Pacific, ‘flanges’ control the escape of vent fluid, leading to the strongest thermal gradient on Earth, whilst in some Atlantic vents ‘beehive diffusers’ are found (Van Dover, 2000). The hydrogen sulfide provides an energy source for microbially mediated primary production by chemolithoautotrophic microorganisms found both free living, forming bacterial mats, and as endosymbionts in certain endemic vent species (Childress & Fisher, 1992). This metazoan fauna, although of relatively low biodiversity, produce a magnificently high biomass of fauna at the vent, surrounded by the very low biomass of the adjacent deep sea (Fig. 1.4f). Hydrothermal vents are also found at subduction zones as well as spreading centres.

The discovery of vents changed the basic paradigms of marine biology for ever. However, sampling and studying of vents could only ever have been carried out by the use of submersibles and more recently ROVs, as the scale at which the sampling takes place is sub-metre and even at centimetre scale.

1.2.4 Into hades

At the other end of oceanic plates, destruction takes places in a subduction zone where, usually, the heavier oceanic plate subducts beneath the lighter continental plate (Fig. 1.1). Because both plates are sinking, we find the deepest ocean on Earth, the trenches, between 6000 and 11 000 m, the best examples of which are found in the western Pacific (Fig. 1.1). Trenches occupy only 1% of the globe and by their tectonic morphology are both deep and very linear. Trenches were first sampled only in the early 1950s by the Danish Galathea and Russian Vitjaz expeditions that used trawls (Jamieson et al., 2010). Piccard and Walsh dived into the Marianas Trench in 1960 in the bathyscaphe Trieste, but after only a brief glimpse of the deepest point on Earth, they dropped their ballast and rose back to the surface. The only other dive to the deepest point on Earth was made in 2012 by James Cameron, who piloted solo the DEEPSEA CHALLENGER submersible. So far, we know that trenches support high bacterial abundance and biomass (Danovaro et al., 2003), as well as an important and diversified benthic fauna (Belyaev, 1989). Sibuet et al. (1988) have also reported the existence of a cold seep fauna in the upper parts of the subduction zone off Japan, and Fujikura et al. (1999) reported the deepest recorded seep at over 7000 m in the Japan Trench.

New technology of sampling such depths is now available and are permitting exciting investigations of the hadal environment. Hybrid remote vehicles are coming on line to be able to sample such environments routinely. Two deep-sea robotic vehicles, Nereus (USA) and Kaiko (Japan), have already reached the deepest parts of the Marianas Trench. To date, some of the most successful sampling has been with landers equipped with baited cameras and traps that have identified taxa not thought to occur at hadal depths (Jamieson et al., 2009).

1.2.5 Special cases

The habitats and ecosystems described above are geographically determined by the tectonic activity or history of the great tectonic plates. There are, however, a number of ‘minor’ ecosystems that are not necessarily geographically determined. These include whale and wood falls as well as seagrass and algal clumps. Generally, these ecosystems are transient, although there is evidence that whale falls may have an impact on the seabed that lasts decades (Smith & Baco, 2003). The main effect of these mini ecosystems is to increase local biomass, although local species diversity immediately adjacent to the organic input may decrease and cause local chemosynthetic activity, particularly in the sediments (Bernardino et al., 2010; Smith & Baco, 2003). There has also been the implication that these ‘minor’ ecosystems are important stepping stones for the dispersal of reproductive propagules throughout the deep sea (Distel et al., 2000). Because of their small scale, these organic inputs can only be examined by the use of submersibles or ROVs.

1.3 Conclusions

Sampling of the deep seabed has changed considerably since the heroic age of deep-sea exploration. The pioneers used trawls and dredges which sampled relatively flat surfaces of sediment or rock. In the 1960s, a move to quantitative determination of the biodiversity of the deep sea led to the development of quantitative samplers, the USNEL box-corer being the workhorse for some 40 years, only recently being replaced by the megacorer. Such corers were limited to sedimentary seabeds and still caused disturbance as they landed. Technology has helped dampen this effect but not eliminated it. The scale of sampling ability was also reduced to sub-metre. Even by the early 1970s, environments with steep slopes and/or rocks, such as canyons and seamounts, were very rarely sampled.

Two notable innovations stimulated the next era of sampling in the deep sea. The development of the submersible Alvin and the movement of oil exploration into offshore waters led to the development of ROVs. With these two aids, sampling could be achieved at small scales and the sub-metre heterogeneity found at cold-water coral reefs, vents and cold seeps could be analysed. Many scientific sampling and analysis packages have been developed and deployed by submersibles and ROVs and with the fantastic improvement in position fixing through GPS, detailed photograph mosaicking of the seabed can occur. In addition, landers and long-term observatories have become an important tool in the armoury of the deep-sea ecologists. In the final analysis, however, there are still areas of the deep sea that are difficult to sample. Canyons with their steep sides, underhangs and strong currents remain a challenge, as do the ocean trenches. Deep-sea ecologists are also very aware of their sampling impact on the deep-sea bed and sampling strategy is now devised to cause the minimal amount of damage to the environment. Sampling technology will continue to develop at all scales within the deep sea, and include a focus on temporal variation. Already we are seeing the establishment of ‘remote sensing’ networks in the Northeast Pacific, and the use of AUVs, both of which will allow access from desk top to the deep sea without the need to board a ship!

Acknowledgements

We acknowledge the support of the Sloan Foundation through the Census of Marine Life Field Programme Chemosynthetic Ecosystems (ChEss). Three reviewers made a number of very useful comments.

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Note

*This chapter was submitted in February 2012.

Chapter 2

Deep-Sea Fauna

Stefano Schiaparelli1, Ashley A. Rowden2 and Malcolm R. Clark2

¹ Department of Earth, Environment and Life Sciences and Italian National Antarctic Museum, Section of Genoa, University of Genoa, Genoa, Italy

² National Institute of Water and Atmospheric Research, Wellington, New Zealand

Abstract

After 150 years of exploration, we now know the deep sea represents the largest complex of ecosystems on our planet which embrace the greatest number of animal species and biomass of the living world. However, there is still a great deal more information that is needed to improve our knowledge of deep-sea faunal dynamics which demands more and better targeted sampling. In this chapter we outline the main biological characteristics of deep-sea organisms, describing aspects of animal life forms, behaviours and adaptations to the deep sea that could affect sampling techniques and survey design. Aspects of spatial and temporal distribution patterns of diversity and abundance are also described for both benthic and pelagic fauna, and examples given of various related sampling issues. The deep sea hosts a huge variety of animal types and faunal communities, with highly variable characteristics. Consideration of these characteristics provides a useful biological context for the sampling techniques that are covered in subsequent chapters of this book.

Keywords fauna, plankton, nekton, benthos, abundance, diversity, temporal and spatial patterns, adaptations, symbioses

2.1 Introduction

Progress toward knowledge of the deep ocean and of the living forms which inhabit it has been slow compared to the study of the more accessible shallow marine environments, hampered by obvious technical, logistic and economic constraints.

The first global biological survey of the deep sea, where the ocean floor was sampled in a systematic way, was undertaken from the HMS Challenger in the years 1872–1876 (Murray, 1895). During this expedition, hundreds of deep-sea stations were completed and a large number of species new to science were collected, resulting in more than 40 volumes of reports. About 80 years after the Challenger, a series of ‘exploration records’ in the deep sea were broken during the decade 1950–1960, which is often remembered as the apex of the ‘heroic age of deep-sea exploration’. In these years, for example, the Galathea 2 expedition (1950–1952) retrieved biological material from the record depth of 10 190 m and the bathyscaphe Trieste (1960) reached the bottom of the Marianas Trench at 10 902 m. However, most deep-sea species had never been observed alive, and their ecologies and behaviours remained largely unknown.

An example of this situation can be found in the illustrations of deep-sea creatures presented in the popular science series ‘The World We Live In’, published by the American magazine LIFE in 1952–1954. Deep-sea organisms had to be painted, as no good photographs were available at the time. In the chapter entitled ‘The miracle of the sea’ (February 1953), the American illustrator James Lewicki depicted deep-sea ceratioid anglerfish and stomiids swimming