No Taxonomy Needed Sponge Functional Morphologies Inform About

Ecological Indicators 129 (2021) 107806
Contents lists available at ScienceDirect
Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind
No taxonomy needed: Sponge functional morphologies inform about

environmental conditions
Christine Hanna Lydia Schönberg a, b, c, d
a
Australian Institute of Marine Science, Indian Ocean Marine Research Centre, Crawley, WA 6009, Australia
b
College of Marine Science, National Sun Yat-sen University, Kaohsiung City 80424, Taiwan
c
Oceans Graduate School and UWA Oceans Institute, Indian Ocean Marine Research Centre, The University of Western Australia, Crawley, WA 6009, Australia
d
Marine Invertebrates, Aquatic Zoology, Western Australian Museum, Welshpool, WA 6106, Australia
A R T I C L E I N F O A B S T R A C T
Keywords: The need to study sponge communities in comparatively inaccessible habitats led to a sponge classification system
Porifera that relies on the strictly functional interpretation of traditional sponge morphologies. The aim is to deliver a
Growth form standardised approach that can optionally be based on imagery and can be applied across all oceans and to any water
Community assessment
depth. The system is designed to recognise community-level changes across time and space. The functional context
Benthic survey
Monitoring
allows a basic interpretation of environmental conditions and may thereby inform on the reasons for observed
Proxy differences in prevailing morphologies. In terms of growth form sponges appear to respond most strongly to the flow
Surrogacy regime and to sediments. Strong turbulent flow will favour low-relief, morphologically simple sponges that are often
Functional diversity structurally reinforced and well attached, such as crusts and simple-massive forms. Laminar flow selects for two-
Hydrodynamic environment dimensionally erect, vertically flattened, usually flexible sponges that are aligned broadside to the current,
Sedimentation inhalant openings (ostiae) pointing upstream, and exhalant openings downstream (oscula). Flow strength is generally
inversely related to number of erect sponges, to body height (except in globular sponges), oscular diameter, branch
number and branch complexity. Where flow conditions reduce or limit access to water exchange and nutrients,
sponges tend to separate in- and exhalants in cup-like forms, reach into the water column as erect and even stalked
forms, and in cases of extreme nutrient limitation the community will consist predominantly of carnivorous sponges.
Globular and fistular sponges are usually abundant where the substrate is dominated by sediments, and where
sediment deposition or movement is high. Fine sediments will often exclude sponges with much horizontal surface
area. Based on these insights, the proposed scheme uses four basic morphologies: functional 1 – crusts, 2 – massives,
3 – cups and 4 – erect sponges. These are further divided into sponges that function as 1 – true crusts, endolithic-
bioeroding, and creeping sponges, 2 – simple-massive, globular massive, composite-massive, and fistular sponges,
3 – cups, tubes, and barrels, and 4 – one-dimensionally, two-dimensionally and three-dimensionally erect forms,
stalked, and carnivorous sponges.
1. Introduction and offshore industries (e.g., Cambridge and McComb, 1984; May, 1992;
Brocx and Semeniuk, 2017) and growing tourism (Hercock, 1999; Collins,
Marine environments in Western Australia (WA) and elsewhere are 2008; Strickland-Munro et al., 2016). Many of these developments require
subjected to continuous and pronounced anthropogenic pressures. Global coastal restructuring and associated environmental assessment. Tradition
change incurs widespread bleaching and benthic mortality (Thomson et al., ally, benthic monitoring assessed sediment, infauna, seagrass and macro
2011; Abdo et al., 2012; Moore et al., 2012; Depczynski et al., 2013; Short algae, coral and some motile macroinvertebrates or those with importance
et al., 2015; Lafratta et al., 2017; Le Nohaïc et al., 2017; Garrabou et al., for fisheries and tourism, but if sponges were surveyed at all, they were
2019; Gilmour et al., 2019). Commercial fisheries cause significant damage commonly grouped without further resolution or listed under “others” (e.g.,
by removing and killing more than the targeted species, with cascading Bremner et al., 2003; Chabanet et al., 2005; Currie and Isaacs, 2005; Emslie
consequences (e.g., Sainsbury et al., 1993; Moran and Stephenson, 2000). et al., 2008; Edgar and Stuart-Smith, 2009). Therefore, our knowledge on
Moreover, infrastructure in WA is rapidly expanding into marine environ sponges and other filter feeders is still rudimentary in this context (e.g., Fig.
ments, by coastal development and urbanisation (e.g., Kullmann, 2014), in- 4 in Costello et al., 2010; Tab. 1 in Schönberg and Fromont, 2012;
E-mail address: [email protected].
https://doi.org/10.1016/j.ecolind.2021.107806
Received 18 May 2020; Received in revised form 21 December 2020; Accepted 8 May 2021
Available online 17 June 2021
1470-160X/© 2021 The Author. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
C.H.L. Schönberg Ecological Indicators 129 (2021) 107806
Kirkendale et al., 2019). This situation is changing, however. Sponges are sponges that were matched to skeletal characters and thereby linked to
increasingly recognised and assessed as key benthic organisms with sig confirmed taxonomy at the species level.
nificant biological importance in many marine habitats, and for their However, even without taxonomy, imagery can still allow spatial
ecological roles and bioindicator functions (e.g., Wulff, 2001; Przeslawski and temporal comparison of sponge assemblages by recognising and
et al., 2008; Powell, 2011; Kenchington and Hutchings, 2012; Carroll et al., describing patterns within a community or at a given point in time, i.e.
2014; Althaus et al., 2015). This led to repeated recommendations for via frequency of different sets of morphologies or growth forms before
consistent inclusion of sponges in monitoring programs (Wulff, 2001; Bell and after an impact or across environmental gradients. Sponge mor
et al., 2006, 2017; Bell, 2007a; Berman et al., 2013; Schönberg, 2015a). At phologies were previously mainly investigated for other reasons,
this stage, however, widely contrasting reports on the status of sponge predominantly in the context of taxonomy (e.g., van Soest, 1989;
communities exist and further highlight the need for more generally Chombard and Boury-Esnault, 1999) or with a mathematic or
applicable, large-scale surveys that include sponges (e.g., Gaino et al., 1992; computational interest (e.g., Kaandorp, 1991; Kaandorp and de
Pérez et al., 2000; Wulff, 2006a, 2006b; Stevely et al., 2010; Wulff, 2013; Kluijver, 1992; Becerro et al., 1994; Abraham, 2001; Kaandorp et al.,
Bell et al., 2018). 2008). Yet some studies used morphologies for community assessment
Mounting evidence attests to extraordinary and highly diverse sponge (e.g., Lawler and Osborn, 2008), and some discussed form and func
habitats around Australia’s coasts (Hooper et al., 1999; Alvarez et al., 2002; tion as a reflection of or response to environmental conditions (e.g., de
Hooper et al., 2002; Hooper and Kennedy, 2002; Hooper and Ekins, 2004; Laubenfels, 1936; Wilkinson, 1988; Wilkinson and Cheshire, 1989;
Ward et al., 2006; Pitcher et al., 2007; Sorokin et al., 2007, 2008; Sutcliffe Schmahl, 1990; Aerts and van Soest, 1997; Aerts, 2000; Bell and
et al., 2010; Barnes et al., 2013; Przeslawski et al., 2013, 2014, 2015; Currie Barnes, 2000a; 2000b; 2000c; Gerovasileiou et al., 2017; Bell et al.,
and Sorokin, 2014), and especially along WA’s coasts (Fromont, 2004; 2002b). Therefore, the strategy of characterising sponge communities
Fromont et al., 2006, 2011, 2016; Fromont and Vanderklift, 2009; Heyward through predominant morphologies is not new. Yet hitherto used
et al., 2010; Williams et al., 2010; Schönberg and Fromont, 2012; Fromont approaches, terminologies and classification systems varied widely or
and Sampey, 2014; Schönberg et al., 2015). However, sponge species were not clearly defined, thus preventing comparison across different
identification is often seen as being difficult (e.g., Knowlton, 2000; studies (Suppl. 1). Most authors appear to uniformly use the terms
Schönberg and Beuck, 2007), and full taxonomic assessment lags behind “encrusting”, “repent” or “globular”, but beyond that the terminology
the sampling effort (e.g., Pitcher et al., 2007; Hooper et al., 2013). Sponge is inconsistent and sometimes confused. Depending on the study,
taxonomy strongly relies on expensive physical samples for spicule and massive sponges may or may not include cups and branching mor
skeleton analysis, processes that commonly require a large time and salary phologies, and sometimes they are part of the category “upright”. The
investment and not always lead to reliable identifications (e.g., Ashok et al., term “lobate” has been widely implemented for massive and branch
2018; Marlow et al., in press). Many of the above studies thus employed the ing sponges alike but was never adequately defined and appears to
use of operational taxonomy units (OTUs), when sponges were taxonomi refer to very different morphologies (e.g., Swearingen III and Pawlik,
cally distinguished within the frame of a given study, but not fully identified. 1998; Barnes and Bell, 2002; Kefalas et al., 2003; Neves and Omena,
This means that meaningful comparisons can be made within a given study, 2003). A more uniform approach to sponge morphologies would be
but not usually between studies (e.g., Schönberg and Fromont, 2012; Hooper desirable, as well as a better understanding of the biological context
et al., 2013). that selects for certain growth forms. Bell (2007b) proposed imple
At other times, only underwater imagery is available to analyze sponge menting field surveys by investigating sponge biodiversity, as well as
communities. WA field conditions do not readily facilitate physical sam their growth forms with respect to function. However, the format of
pling, especially not with SCUBA divers in the water. The occurrence of this particular proposal involved 39 different morphologies, a number
large sharks (e.g., Gibbs and Warren, 2015; McAuley et al., 2016), croc that may be somewhat impractical for environmental assessment in
odiles (e.g., Mawson, 2004; Caldicott et al., 2005) and dangerous sea general. Moreover, the functional roles to be assessed at this level of
jellies (e.g., Gershwin, 2005), extreme tidal currents in the north (e.g., detail require prior knowledge about the sponges’ biologies and may
Wilson et al., 2011; McInnes et al., 2016; Gruber et al., 2017), sites with thus be unsuitable for use by a wide range of agencies. Despite some
high turbidity (e.g., Semeniuk, 1993; Lafratta et al., 2017) and hazards studies that evaluated the ecological potential of looking at sponge
due to expanding industrial activity and ship traffic (e.g., Blakeway et al., growth forms (e.g., Schönberg et al., 2005; Bell, 2007b; de Voogd and
2013; Wilson et al., 2019) restrict diving opportunities that would enable Cleary, 2007, 2009; Gerovasileiou et al., 2017), the science commu
representative tissue sampling for reliable sponge taxonomy. The use of nity has not yet widely employed the interpretation of sponge mor
autonomous or towed camera equipment is often preferred to capture still phologies with the general aim of generating further information
and video imagery at no risk for divers and as a means to survey larger about prevailing habitat conditions. Yet sponges respond to their en
areas in less time, thus potentially creating larger datasets (e.g. Barrett vironments, and a predominance of certain growth forms can yield
et al., 2010; Althaus et al., 2015). In consequence, surveys conducted with information about their functions and about environmental condi
towed cameras became increasingly common, and requests for sponge tions that select for them (e.g. de Laubenfels, 1936; Bell and Barnes,
identifications from underwater imagery developed into a persistent issue. 2000a; Schönberg and Fromont, 2012; Schönberg, 2016a). This
However, due to a high level of morphological plasticity within many insight has led to the proposal for a standardised classification scheme
species (e.g., Hill, 1999; Duran and Rützler, 2006; López-Legentil et al., defining sponge growth forms explicitly in the context of ecological
2010; DeBiasse and Hellberg, 2015) and at the same time a large potential function, providing a tool to characterise sponge assemblages and a
for similar habits and morphology in different species (e.g., Solé-Cava and proxy for environmental conditions (Schönberg and Fromont, 2013,
Boury-Esnault, 1999; Schönberg, 2002a; Schönberg et al., 2005; 2006; 2014; Althaus et al., 2014, 2015; Suppl. 2). To date, this concept has
Xavier et al, 2010; Leal et al., 2016; Mote et al., 2019), sponges can neither only been employed for surveys in Australia (e.g., Schönberg and
be reliably identified from images that lack finer detail, nor without ex Fromont, 2012; Carroll et al., 2014; Przeslawski et al., 2014; Althaus
perts with local knowledge and earlier reference samples. This is espe et al., 2015; Bewley et al., 2015; Abdul Wahab et al., 2017, 2018;
cially true in areas such as WA, where many sponge identifications are James et al., 2017; George et al., 2018). These studies relied on earlier
OTUs and where respective biologies remain largely unexplored. Further, versions of the scheme that were later changed and adjusted, or the
until recently no guides or in situ reference images existed for live WA scheme was at times incorrectly used, misunderstanding some of the
2
concepts (see details in Suppl. 1). As the proper application of it and and to what extent they may covary with other factors, but whatever in
its underpinning have not before been explained in detail, the purpose formation became available was listed as part of Suppl. 2. Factor 1 was
of the present paper is to formally introduce the concept of sponge here regarded as one of the strongest drivers (e.g., Hiscock, 1983; Carballo
functional growth forms as a globally compatible tool in environ et al., 1996; 2008; Barnes and Bell, 2002; Bell, 2007b) and was more
mental assessment. The paper provides sufficient detail and examples closely considered by comparing possible effects of
for the scheme to be used in widely differing contexts.
i. stagnant water versus high energy flow,
2. Material and methods ii. persistent versus acutely disruptive flow, and
iii. laminar flow such as caused by tides or by seabed structures
The present concept or classification scheme of using functional causing a channel effect versus chaotic and turbulent flow such as
sponge morphologies for benthic surveys grew over a number of years. from crashing waves.
Known sponge growth forms and related terminologies were reviewed
using pertaining literature (e.g., Boury-Esnault and Rützler, 1997; and As a result, the development of the classification scheme was mostly
further references listed in Suppl. 1). Around 300 publications were based on factors 1 and 2 as the key drivers. And in addition, flow con
screened, and relevant information was extracted and synthesised for ditions were assessed in further detail. Related patterns apparent in the
patterns in sponge functional morphology and their bioindicator value main sponge morphologies were summarised and specifically set in the
(Suppl. 2). Originally the focus lay on marine demosponges and on context of their function within a given environment and in view of the
imagery of shelf sponge communities between the intertidal and ca. 200 ecology of sponges. Based on this, a range of “functional morphologies”
m water depth, mostly from sites around the northern half of Australia were distinguished for sponges at different levels of resolution for
between Perth and Townsville. This focus was gradually expanded. New scoring. These morphologies were again tested and adjusted as part of
or revised definitions and terms were created for sponge morphologies ongoing fieldwork in WA and on the Great Barrier Reef (e.g., Heyward
that were not yet clearly described, and resulting concepts evaluated et al., 2010; Schönberg and Fromont, 2012; at that time based on 6
during fieldwork in WA and on the Great Barrier Reef. Emerging cate different morphologies) and by consulting the literature (Suppl. 1–2).
gories and functional interpretations were further developed during During a sponge classification workshop held by the University of
discussions with international colleagues familiar with sponges in situ in Western Australia during the 2013 World Sponge Conference this pilot
different oceans, but also with non-sponge experts as potential users and scheme was first made available to the public and tested by a range of
with people who have long-term experience with surveys conducted by potential users from different countries (Schönberg et al., 2016; the
underwater imagery. system then relied on 4 principal morphologies and 12 sub-categories).
Examples for sponge taxa fitting various morphologies were assem The workshop participants were asked to score a number of underwater
bled. Formats and validities of any species name used in the publication images to assess whether the chosen morphologies sufficed to describe
and the supplementary material were checked in the World Porifera common sponge growth forms and whether different users with expe
Database (van Soest et al., 2020) and itemised together with the most rience from different benthic habitats would reliably recognise the same
common growth form per species as Suppl. 3. forms. The scheme was then further edited, which resulted in 4 basic,
Various environmental or anthropogenic factors were considered overarching morphologies that can be scored to finer resolution as 14 or
that may have an impact on sponge morphologies and that may select 21 categories to also include sponge classes beyond the Demospongiae
for certain growth forms (for further details see Suppl. 2); they were here and from other sites than Australia. Finally, definitions were created and
considered for horizontal substrates only for clearer pattern recognition used for recommendations for surveys and monitoring purposes, and
and standardisation, but some of the listed factors also create commu CAAB numbers were allocated to different categories (Codes for
nity patterns on inclined, vertical or inverted substrates: Australian Aquatic Biota; http://www.marine.csiro.au/data/caab/).
These numbers create consistency by making it possible to match the
1. Hydrodynamics (flow structure and strength, mixing) same groups across different resolution levels and over time in cases for
2. Sedimentation (turbidity, sediment deposition, abrasion) which terminology was changed or the scheme was rearranged
3. Nutrients (gradients, anthropogenic eutrophication) compared to earlier versions (e.g., in the CATAMI image classification
4. Physical damage (storms, human activity through fisheries or scheme; http://catami.github.io/). The present classification scheme for
construction) sponges is now published so it can become more widely available and to
5. Substrate type (hard, sandy, muddy bottom) be tried and fine-tuned at global scale, in marine and freshwater envi
6. Biological interaction (predation, competition, symbiosis) ronments, across the entire bathymetric scale and in all climates.
7. Illumination (photosynthetic ability, UV damage; exposed/
covered location) 3. Results and discussion
8. pH (ocean acidification)
9. Temperature (climate, season, climate change, heat events) 3.1. A sponge classification scheme by functional morphologies:
10. Bathymetry (a product of pressure, hydrodynamics, illumination, Definitions in the ecological context
sedimentation)
11. Salinity (gradients, freshwater influx) The present classification scheme is structured in several cascading
12. Oxygenation (saturation state) levels of resolution to suit the needs of different users (Table 1). The
coarsest differentiation employs 4 basic functional morphologies: func
According to Petchey and Gaston (2006) and their thoughts on the tioning as crusts, as massive forms, as cups and as erect forms, each
methodologies in the assessment of functional diversity, the appropri category being further subdivided (Figs. 1–3). Where the sponge mor
ateness, relative importance and prediction value of the above factors was phologies are to be applied as a proxy for environmental conditions, they
evaluated after extracting relevant reports from the literature (Suppl. 2). need to be strictly scored in the context of function, and their resolution
Thereby, factors 1 and 2 were generally judged to exert the most influence should distinguish 14 different morphologies or more, as explained
on sponge growth forms, and that certain sponge morphologies appear to below (including the morphologies numbered at integer-level in
be indicative of environmental conditions governed by them. Factors 3–7 Table 1). The maximum of distinguished morphologies was consciously
are also thought to be able to affect sponge morphology to some degree, kept to a manageable number at the finest resolution, and a total of 21
but these are less well understood. It is not known whether and how the different forms is here explained. However, it is very unlikely that all
rest of the listed factors may select for predominant sponge growth forms categories occur at any given site at the same time, so the number
3
Table 1
The tabulated structure and hierarchy of the classification system based on sponge functional morphologies. There are four basic forms: functioning as encrusting,
massive, cup-like and erect (in frames). These are subdivided into some further morpho-functions for finer scoring as indicated by numbering. When using the scheme
in order to resolve for environmental conditions, it is recommended to assess sponge morphologies with a resolution of a minimum of 14 separate categories (categories
in the first column, numbered by integers). As numbering, terms and group-allocations changed during the development of the system, allocated CAAB numbers (Codes
for Australian Aquatic Biota) generate consistency when matching various assessments. CAAB numbers recently added for adjustments made with this publication are
marked with an asterisk (and earlier versions can be compared to this one in Suppl. 1). The colour scheme in the PDF version of blue – red – green – yellow for the
groups encrusting – massive – cup-like – erect and their subgroups is carried through the rest of the paper in the electronic version, but is not displayed in hardcopy.
Example images for the different categories are provided in Figs. 1-3 and Suppl. 4–6.
handled during fieldwork will usually remain well below 20. Of course, Functional context: Sponges functioning as crusts have the lowest
there are intermediate morphologies and functions, and the environ profile of all listed forms and do not experience much drag by flow
mental context should rigorously be applied as the predominant factor (Denny et al., 1985). They are anchored across a proportionally very
to decide the scoring result. As an aid to facilitate such decisions, a basic large area due to their shape, which makes them very resistant to
layman’s key was added in form of a flow chart for scoring (Table 2), but damaging water movement (Bell and Barnes, 2000a; Wulff, 2006a;
further details are explained below. Gochfeld et al., 2020). The more damaging the local flow regime is, the
less three-dimensional structure and the more flattening can be seen in
3.1.1. Sponges functioning as crusts (CAAB 10 000901; Fig. 1A) sponges (de Laubenfels, 1936; Bell and Barnes, 2000a; except in balls,
Definition: Sponges that function as a crust sensu lato combine see Suppl. 2). Fully attached encrusting sponges will thus be best
encrusting sponges in the wider sense with creeping sponges. They have equipped to persist in environments frequently exposed to unpredictable
a very low profile and extend in a layer parallel to the substrate. Their and/or high-energy hydrodynamic conditions such as at exposed coasts
area is significantly larger than their height, and they have a paucity of where waves break, and they will be more likely to survive storm events,
three-dimensional or vertical structure in comparison to horizontally experiencing less damage than other morphologies (Bell and Barnes,
extending tissue. In- and exhalant openings are on the same plane, as the 2000a; Wulff, 2006a). However, when occurring on horizontal surfaces,
body shape does not allow distinct separation of them, but they may be the shape of encrusting sponges creates a high risk of being smothered
arranged in different groups, e.g. in rows or in patchily distributed by sediment deposition, i.e. they could quickly become entirely covered
clusters. More example images are figured in Suppl. 4–5. by sediment. Many crusts do not normally tolerate fine sediments unless
4
they have particle-repellent mechanisms (Lawler and Osborn, 2008; encrusting sponges appear to be more common in exposed coastal set
Schönberg, 2016b) or can actively clean their surfaces (e.g. Könnecker, tings, and most occur to roughly − 200 m water depth (de Laubenfels,
1973). Alternatively, sponges functioning as crusts can find refuge on 1936; Maldonado and Young, 1996; Mendola et al., 2008; Schönberg
vertical or inverted surfaces (e.g., Bell and Barnes, 2000a; 2000b; and Fromont, 2012). Where they are reported to occur deeper than
2000c). When occurring on e.g. vertical substrate, however, their pres − 200 m, they are usually found on inclined, vertical or inverted surfaces
ence will no longer inform on sediment pressures and can only be used as where they do not experience sedimentation (e.g. see Fig. 8 and Video 5
proxy for the flow regime. Overall, predominance of crusts generally in Santín et al., 2018).
implies strong, mostly turbulent, potentially damaging flow that resus Subgroups: Category 1 – Encrusting sponges in the wider sense,
pends and removes sediments from their surfaces. Due to their favour sensu lato (CAAB 10 00922) divide into the categories 1.1 – true crusts,
able filtration : surface ratio (Bibiloni et al., 1989) they can also exist in i.e. encrusting sponges sensu stricto (CAAB 10 000902) and 1.2 –
flow-reduced, nutrient-poor habitats if sedimentation is low, but endolithic, bioeroding sponges (CAAB 10 000921). The true crusts are
Fig. 1. Examples of sponge functional morphologies

in environments that select for certain growth forms –
communities functioning as encrusting or massive. A –
Creeping (left, green) and encrusting (right, red)
sponges often occur in areas with turbulent flow, in
this case in the Mumbai intertidal, likely due to waves
in shallow water. Creative commons photograph by
Pradip Patade (2019). B – Simple-massive sponges
such as these eastern Mediterranean Spongia (Spongia)
officinalis can occur in a wide range of conditions that
do not tend to the extreme, but due to the mixed in-
and exhalant openings sufficient flow is needed to
wash away the exhaled water. Photograph by Thanos
Dailianis©, with friendly permission. C – Ball-shaped
sponges such as Tethya spp. can occur in clear and
turbid waters, usually in strong flow conditions, here
in the exposed intertidal of southern New South
Wales. Photograph by Paul Whitington© (2019), with
friendly permission. D – Fistular sponges such as the
pictured Spheciospongia cf. inconstans at Singapore
often live endopsammic, i.e. mostly buried in sedi
ment. Fistular sponges are usually indicative of mov
ing sediment and high sediment deposition rates.
Photograph by Swee-Cheng Lim©, with friendly
permission. (For interpretation of the references to
colour in this figure legend, the reader is referred to
the web version of this article.)
5
thin crusts (CAAB 10 000923; Fig. 1A) and thick crusts (CAAB 10 Schönberg pers. obs. for a Cliona celata complex sponge from the
000924). Thin crusts have a tissue thickness of very few mm and best central Great Barrier Reef), but this is uncommon. Tolerance of being
represent the traditional understanding of encrusting sponges. They covered by a sediment layer varies with species and sediment prop
display the best-defined functional traits and are the most reliable erties, with finer sediments being more damaging (Siebler et al., 2013;
proxies for high-energy environmental flow conditions. They are those Schönberg pers. obs.). However, due to erect spicules embedded in
that usually predominate at sites with strong, damaging, unpredictable their ectosome all clionaid species have a velvety surface that appears
hydrodynamic conditions that exclude more delicate or vulnerable to be particle-repellent so that they are tolerant to sedimentation
morphologies (Schmahl, 1990; Bell and Barnes, 2000a). Thick crusts or (Schönberg, 2015b). Like true crusts, endolithic sponges may some
low cushions of few mm to around 1 cm in thickness have similar times be scored in a different functional context, e.g. if they inhabit the
properties with regards to flow as thin crusts, but their often slightly entire skeleton of a massive coral they should be scored as simple-
more convex form or slightly raised papillae render them a little less massive (Fig. 4C), if they fully penetrate a branching coral, they
vulnerable to sedimentation. The definition how thick a crust should become erect-branching. They may often simply be mistaken as true
be to fall into either thin or thick crusts varies between publications (e. crusts, which will not change their functional context or the scoring
g., in Bell and Barnes, 2003 thick crusts are > 2 mm thick) and may result for environmental conditions. Widely distributed examples are:
require quantitative research for a better characterisation of the cat Cliona spp., Pione spp., Cliothosa spp. and tetractinellid bioeroders (see
egories. There may be a trade-off between flow-resistance and growth also Suppl. 5.1).
rate, as some thickly encrusting sponges have been found to grow Category 2 – Creeping or repent sponges (CAAB 10 000917; Fig. 1A)
faster than thinly encrusting sponges (Ayling, 1983). Examples for thin hug the substrate, but they form a horizontal branching or meandering
crusts are e.g.: Timeidae, Plakortis simplex, Spirastrella spp., Terpios network or patchy crusts that are often weakly attached. Therefore, they
spp., Merlia spp., Halicnemia patera, Hymedesmia (Stylopus) coriacea, commonly function as hybrids at the crust-branching interface and can
Clathria (Microciona) aceratoobtusa. Examples for thick crusts are e.g.: develop erect portions. Like other crusts, creeping sponges can quickly
Spirastrella spp., Placospongia spp., Acanthoclada prostrata, Phorbas be smothered if sediments were to build up around them, but by
fictitius, Crambe crambe (see also Suppl. 5.1). Please note that some of developing erect parts they can escape the suffocating layer. Depending
the species listed as examples may sometimes belong to more than one on the size and the frequency of the erect parts and the degree of burial,
morpho-functional category and may display a range of morphologies creeping sponges may alternatively be scored as erect-branching or
depending on conditions. fistular. However, creeping sponges still have a much larger attachment
Due to their sheltered position and good attachments, insinuating area than erect-branching ones and may not commonly be endopsammic
sponges that grow into existing cracks (e.g. Mycale laevis), grooves and like fistular ones. The adaptation of creeping sponges to survive in un
depressions should probably be counted into the encrusting sponges like predictable, high-energy hydrodynamic conditions appears to rely less
the endolithic bioeroders, but at times they can be functionally closer to on firm attachment or direction of growth and more strongly on either
creeping forms (e.g. some small Haliclona spp.) and decisions should be being more elastic due to high spongin content or due their fast growth
made on case-to-case basis. When using sponge growth forms as envi rates and their high capacity to fragment, heal, re-attach and regenerate.
ronmental proxies, the functional context needs to be strictly more These are functions commonly found in “ropy” or creeping sponges
important for scoring than their mere shape. If crusts develop erect (Wulff, 1990, 2006a). Creeping sponges are not usually as dependent on
structures such as in Polymastia or Ciocalypta spp. and become partially firm, hard substrate as other encrusting sponges, as some can extend
buried in sediment, they rather function as fistular than as encrusting over rubble or even sediments, which they bind (e.g. Carter, 1882 for
sponges. Thin crusts can occasionally adopt the function of thick crusts or Callyspongia (Cladochalina) tenerrima, Mycale (Mycale) laevis and Spongia
even massive sponges if they grow over rounded stones or rocks that give (Spongia) officinalis (Fig. 1B, 5A–D); Biggs, 2013 for Niphates erecta and
them an overall convex shape, in which case they should be scored ac Aplysina spp.). They are overall more variable in their ecological re
cording to this functional context, not as thin crust. Crusts growing around quirements, functions and forms than many of the other listed mor
erect or massive structures are counted according to the shape they then phologies. As a consequence, they can occur in diverse and less
inherit: e.g. as simple-erect if they coat a whip-like gorgonian, as stalked predictable environments and can adjust to different prevailing condi
or erect-branching if they coat a stalked or tree-like structure, and as tions, such as different substrate types. Further examples of creeping
simple-massive when coating most of a rock – these crusts are no longer sponges are e.g.: Agelas conifera, Callyspongia (Callyspongia) fallax,
restricted to the boundary layer environment and stop functioning like Clathria (Thalysias) virgultosa (Fig. 7D), Haliclona (Gellius) cymaeformis,
crusts in terms of flow conditions (Fig. 4A-C). Conveniently, this approach Hyrtios erectus, Pseudoceratina purpurea, Petrosia (Petrosia) ficiformis,
facilitates standardisation when scoring sponges from imagery without Petrosia (Strongylophora) strongylata (see also Suppl. 5.2).
taxonomic knowledge – the visual impression will deliver the right
answer. 3.1.2. Sponges functioning as massive forms (CAAB 10 000903; Fig. 1B-C)
Category 1.2 – Papillate (“alpha”) or sheet-like (“beta”) endolithic, Definition: Compact massive sponges are very roughly as wide as
bioeroding sponges (CAAB 10 000921) are a special category within high. Sponges functioning as massive very often, but not always, have
the crusts. Within the substrate they erode, some species can be rela most of their body mass as one coherent piece of tissue. However, they
tively three-dimensional, but where they are exposed to the environ can also be amorphous and irregular in shape or can be composed of
ment, they experience conditions like a crust. They can usually merged subunits that overall form a common mass. Most massive
withstand the same extreme flow regimes as thin crusts and appear to sponges do not distinctly separate in- and exhalants on different sur
be resilient to storm damage, grow faster and are often more common faces. Therefore, barrels are here excluded from the category “massive”:
and more diverse at sites with good hydrodynamic mixing (Schönberg, While their body shape and mass suggest they belong to the “massives”,
2001; Schönberg and Burgess, 2013; Schönberg unpubl. data). How one of their most important functions manifests in separated in- and
ever, they cannot colonise just any kind of hard substrate and depend exhalant surfaces and more strongly relates to the cup-like sponges
on calcium carbonate or organic substrate with a high content of cal (Fig. 5F-G). Further examples are displayed in Suppl. 4–5.
cium carbonate (Schönberg, 2002b, 2008). In this way they are bio Functional context: As an entire group, functionally massive sponges
indicators for the presence of calcium carbonate materials. Their upper are not as good bioindicators as are other morphologies, and they
surfaces bear both, in- and exhalant openings in close proximity, commonly occur across a relatively wide range of environmental condi
although these can occasionally form groups, fields or lines. Papillate tions. Jackson (1979) confirmed this impression through calculations
sponges that inhabit flat, horizontal pieces of substrate can at times using approximated parameters: The massive “growth form represents a
separate inhalants (bottom surface) from exhalants (upper surface; series of adaptive compromises for almost all shape parameters
6

in environments that select for certain growth forms
– cup-like communities. A – A sponge community
that is strongly dominated by wide cups mingling
with erect sponges at Bare Island (Sydney, E
Australia) in –22 to − 24 m suggests reduced sedi
mentation pressure and benign flow conditions.
Image extracted from video by Thierry Rakotoar
ivelo© (2019), with friendly permission. B – Xesto
spongia testudinaria barrels with separate in- and
exhalant areas were conspicuous in a filter feeder
community in − 11 m in the Pilbara (NW Australia)
that was characterized by fine sediments and high
turbidity and sedimentation rates. Ianthella basta on
the right was curled into tubes and chimneys. C – A
glass sponge community in − 860 m at Socorro Is
land at the Revillagigedo Archipelago (Mexican E
Pacific). The dominant sack-like morphology sug
gests reduced flow conditions. Screenshot from
video by Ocean Exploration Trust© (2017), with
friendly permission from Nautilus Live, Ocean
Exploration Trust.
7

in environments that select for certain growth forms –
communities with erect sponges. A – Palmate, two-
dimensionally erect sponge community at Bare Is
land, Sydney, E Australia, that imply predominantly
laminar flow in the right-left direction of the photo
graph. B – Mostly three-dimensionally erect-branch
ing sponges in Sydney Harbour suggest reduced flow
conditions. The prevailing currents may be mostly
laminar, as two-dimensional sponges appear scattered
in between. Creative commons photographs A and B
by John Turnbull (2014), with friendly permission. C
– Delicately stalked glass sponges at Ridge Seamount
of Johnston Atoll in − 2360 m, with their convex sides
pointing into the main current, presumably a current
with low flow speeds. In this depth currents are usu
ally strongly reduced, and sponges have to reach far
into the water column. Screenshot of a video by
NOAA Office of Exploration and Research (2017),
creative commons. D – The carnivorous harp sponge
Chondrocladia (Symmetrocladia) lyra, Hadal Wall at
the Mariana Trench. Screenshot of a video by NOAA
Office of Exploration and Research (2016), creative
commons. E – The carnivorous ping-pong tree sponge
Chondrocladia (Chondrocladia) grandis off Baffin Is
land, Canada. NOAA Office of Exploration and
Research (2015), creative commons. Presumably,
both sponges occurred in areas with little access to
food suitable for filter feeding, thus specialising in
carnivory.
considered.” He reasoned that massive and encrusting forms together will et al., 2007). Most massive sponges are not overly fragile, and some robust
likely only dominate if food and other staple resources are in abundant sponges can withstand turbulent flow without damage (e.g., Bell and
supply and disturbance levels are low, so that sessile organisms of a more Barnes, 2000a). Yet their structure can fail in strong currents, and they can
simple form can outcompete more erect forms. However, it may in fact be be fragmented or detached during storm surges, depending on their shape
the other way around, i.e. that erect forms persevere under more restricted and attachment area, and breaking waves select against them. Massive
conditions, but more observations are needed. Different species will prefer sponges have significant area in form of upper surfaces that will collect
different flow conditions, and most massives would require enough flow some sediment, but usually they grow up from the bottom far enough to
to quickly remove their wastewater as they either do not bundle their avoid smothering and have a significant amount of vertical or sloped
exhalant stream, or do not do this very well (e.g. Rhopaloeides odorabile surface that will remain sediment-free, or have erect fistules that can reach
was more abundant at high-flow sites on the Great Barrier Reef; Bannister through layers of sediment. Massive sponges appear to have commonly a
8
Table 2
Decision flow chart or layman key for scoring the 14 sponge functional morphologies that can be used as a proxy for environmental conditions. The scoring context
needs to be strictly functional.
bimodal bathymetric distribution, with a shallower, upper-shelf group for settlement, and with moderate to strong, predictable flow (e.g.,
and a deeper group that reaches beyond the shelf edge (Maldonado and Carballo et al., 1996). Examples are e.g.: Asteropus niger (Fig. 7E), Pet
Young, 1996; Schönberg and Fromont, 2012), an observation that pres rosia (Petrosia) ficiformis, Fascaplysinopsis reticulata, Hyrtios cavernosus
ently remains unexplained and may need to be better matched with (Fig. 7B), Rhopaloeides odorabile, Spongia (Spongia) officinalis (Fig. 1B,
morphologic traits. 5A-D; see also Suppl. 5.2).
Subgroups: Category 3 – Simple-massive sponges (CAAB 10 000904; Category 4 – Balls or globular sponges (CAAB 10 000905; Fig. 1C)
Fig. 1B) are best suited to mid-range environmental conditions. They are occur in a large variety of conditions, some of which would be harmful
not well adapted to survival in stagnant water, because their in- and to other sponge morphologies. For example, spirophorine balls are
exhalants are not as clearly separated as e.g. in barrels (Fig. 5). This common at high energy sites with turbulent flow, are drag-resistant or
simultaneously means that the oscules are usually scattered, which nestle in concave parts of the substrate that reduce hydrodynamic
makes their exhalant stream weaker than in sponges with oscular pressures, and some have a high potential for regeneration after physical
grouping (Fry, 1979). Without sufficient flow, they would risk to re- damage (Schmahl, 1990; Denny, 1994; Barnes, 1999; Siebler et al., 2013
inhale their own wastewater (Bidder, 1923; Fry, 1979), however, – but Wulff, pers.comm.: balls commonly regenerate slower than other
some sponges can apparently choose which particular oscules to use morphologies). Some astrophorine balls have been found under reduced
depending on existing currents (Patterson et al., 1997). Moreover, flow conditions, however (Cleary and de Voogd, 2007). Unlike the other
depending on the ambient flow, simple-massive sponges can have more growth forms, balls become smaller and flatter in low flow and are larger
spread-out or more apically grouped exhalants (Fig. 5A-D). Violent hy at exposed sites (McDonald et al., 2002; Meroz-Fine et al., 2005; Lawler
drodynamic conditions can dislodge massive sponges (Wulff, 1999, and Osborn, 2008). Especially tetractinellid balls are known for their
2006a), especially if they have a low spongin content. Once unattached resistance to sedimentation, and many species maintain an external
their survival potential is low, unless larger fragments are stabilised crust of sediments and algae or agglutinate coarse materials that adhere
(Wilkinson and Thompson, 1997; Bell and Barnes, 2001a; Wulff, 2006a). to their surfaces (Schönberg, 2016a). Unlike many other sponges, many
Simple-massive sponges are usually bulky enough not to be entirely balls can tolerate fine sediments, high sedimentation rates, turbid water
smothered at sites with high sedimentation rates, but their upper sur and even week-long burial in sediment (Rice, 1984 for Cinachyrella
faces can become sediment-covered and may develop anoxic parts or apion; Bell and Barnes, 2000b for Tethya aurantium; van Soest and Rüt
pockets that collect so much sediment that it becomes embedded in the zler, 2002 for the Tetillidae; de Voogd and Cleary, 2007). Yet some
sponge (Schönberg, 2016a; Hoffmann et al., 2004 Schläppy, pers. ball-shaped sponges have also been reported to prefer or to require clear
comm.). They do not usually tolerate soft sediments (Lawler and Osborn, water (e.g., Carballo et al., 1996 for Tethya aurantium). Like barrels,
2008) and can be comparatively vulnerable to diseases (Wulff, 2006b; some globular sponges spatially separate incurrent ostiae from excurrent
Abdo et al., 2008). In general, simple-massive sponges will do best in oscula, with the inhalants on their lateral surfaces and the exhalants
low-sedimentation, coarse-sediment environments with rocky outcrops downstream or apically concentrated. However, as balls with mixed, as
9
well as with separated openings both occur in clear and turbid waters, Schönberg, 2016a). Some fistular species such as Tentorium papillatum can
and at high-energy and flow-reduced sites, their most important func keep their surfaces sediment-free (Barthel and Gutt, 1992). Sedimenta
tions seem to be related to their drag-reducing shape and mode of tion, as well as starvation can induce formation of erect parts and pro
attachment, rather than to their feeding and gas-exchange strategies. As cesses in sponges that do not normally display fistule-like structures, such
presently no clear patterns can be reported, future observations may as in some Suberitida, Haplosclerida and Poecilosclerida (Stone, 1970;
help fine-tune the functional niches of this category or possible sub Jones, 1994; Cummings et al., 2020). Even if the sponge is not embedded
groups. Nevertheless, based on what we presently know about the in sediment, occurrence of fistule-like structures is thus a good indicator of
functional ecology of globular sponges, they should probably best be locally permanent or temporally elevated sedimentation rates (Fig. 4F).
scored as a single group, and no attempt should be made to distinguish Fistular sponges combine elements of massive and erect sponges, but the
them into simple-massive and barrel-like sponges according to the dis main body mass of many species can occur both, on top of the substrate,
tribution of their ex- and inhalants until we better understand their wedged in between substrate or buried in sediment (e.g., Schönberg and
environmental requirements. Typical balls are relatively small sponges Lim, 2019), and they often have longer and more pronounced fistules in
that are situated close to the substrate and the boundary layer. Their the latter case (e.g., warty or hillocky to fistular in Spheciospongia spp.;
function will change if they grow on erect structures and are situated Fig. 1D, Suppl. 5.3H, I, N, P, Schönberg pers. obs.). For scoring, endop
much higher in the water column. In that case they may be scored as sammic or sediment-dwelling specimens only showing fistules above the
functioning like stalked sponges (Fig. 4D). Examples for balls are e.g.: substrate differ from branching or palmate sponges by their “branches”
Tethya spp. (Fig. 1C), globular astrophorine sponges such as Stelletta (fistules) being more horizontally distributed and rising from the massive
clavosa, spirophorines such as Cinachyra spp., Cinachyrella spp. or crustose sponge body, rather than originating from a stem. In endop
(Fig. 7H), but also small-bodied, globular sponges such as some Suberites sammic sponges that are largely hidden in the sediment, the fistules can
spp. (see also Suppl. 5.2). look like separate, simple-erect sponges rising from the bottom. Typical
Category 5 – Composite-massive sponges (CAAB 10 000927) are examples of fistular sponges include Oceanapia spp., Ciocalypta spp.,
those that by their overall shape resemble and behave like a massive Coelocarteria spp., Polymastia spp., larger species of the genus Siphon
sponge under the prevailing conditions, but they are really mounds of odictyon, and some Spheciospongia spp. (Schönberg, 2016a).
mesh-like, reticulate or clathrate sponges such as Clathria spp. or The unattached, disc- or inverted cup-shaped sponge Xenospongia
composed of closely merged subunits such as tightly clustered branches patelliformis is here regarded as an unusual member of this category
or densely joined thick fans that are arranged in three dimensions (Fig. 6). While it does not have pronounced fistules, Sarà (2002)
(Fig. 4E). Overall, they largely function like simple-massive sponges in described its upper surface as “minutely tuberculate or conulose” and as
that they do not usually have a clear separation of in- and exhalants, but having “small rounded tubercules and oscules on slight prominences”.
clathrate sponges are more delicate and more vulnerable in strong Moreover, the upper side is convex (Fig. 6A-B; Fig. 9A in Sutcliffe et al.,
currents, and due to an increased surface rugosity clustered sponges 2010), so that the sloped, hispid surface may allow sediment to roll off
would likely accumulate more sediment than simple-massive sponges. (Fig. 6A; Schönberg, 2015b). The sponge lives on sandy bottoms and
They also have an increased surface area compared to simple-massive rests on the rim of the convex disc, which is fringed with megascleres
sponges, which may enhance their feeding efficiency. Examples are e. extending from the sponge and prevent the sponge from sinking into the
g.: Acanthella pulcherrima, Agelas dispar, Dragmacidon reticulatum, Ircinia substrate (Fig. 6D-E). At the same time the lower, inner, concave surface
felix, Stylissa massa. is weighed down by embedded sand grains to 2/3 of the sponge’s
Category 6 – Fistular sponges (CAAB 10 00908; Fig. 1D – called thickness (Sarà, 2002; Sutcliffe et al., 2010), presumably to prevent the
cryptic-massive in earlier versions), mostly the so-called endopsammic sponge from being flipped over by currents. By having raised oscules on
sponges, are sediment specialists with high bioindicator value (e.g., de the central part of the upper, concave side (Fig. 6B), and by incorpo
Laubenfels, 1936; Rützler, 1997; Cerrano et al., 2002; Schönberg, 2016a, rating sediment for anchoring (Fig. 6A, C, E), this sponge thus matches
and references therein). They are well suited to environments with high basic morphological patterns of fistular sponges, as well as the function
sedimentation rates and moving sediments and are adapted to being of being highly adapted to sediment-dominated environments. Despite
covered by or being partly or almost entirely buried in sediment. Many are the flat body of this sponge, this interpretation may be supported by
also tolerant to intertidal environments where the sponges’ upper parts other weakly attached or unattached, sediment-dwelling sponges with
may become exposed to air (e.g., Schönberg, 2000; 2001 for Siphon spicule fringe that also have fistules, such as e.g. Polymastia grimaldii and
odictyon mucosum; Vinod et al., 2009 for Spheciospongia inconstans; see also Polymastia hemisphaerica (Plotkin et al., 2018). X. patelliformis occurs in
Fig. 1D; Lim et al., 2008; Schönberg and Lim, 2019 for Spheciospongia spp. shallow, sandy environments with variable oxygen saturation (Sutcliffe
and Coelocarteria singaporensis). In most cases their main body can best be et al., 2010).
described as massive, sometimes as encrusting to cushion-shaped, but for
their ecological function it is more important that they have raised, 3.1.3. Sponges functioning as cups and cup-like forms (CAAB 10 000909;
elevated or erect, knuckle, wart- or finger-like parts or pronounced fistules Fig. 2)
on their upper surface, or sometimes strongly collared, extended oscules Definition: Cup-like sponges have a concave upper surface. Most
that reduce the risk of sediment entering the aquiferous system. Exhalant can efficiently separate their in- and exhalant openings, with inhalants
fistules are hollow or contain large canals. If inhalants are vertically on the outer or lower surface, and exhalants on the upper, inner sur
extended, they can be more compact and may be terminally closed and face (Bergquist, 1978; Fry, 1979; Trammer, 1979). This separation
appear solid in cross section, with much more narrow canals. Fistular may not always be complete, but it is generally more strongly pro
sponges usually have basal or endolithic root-like tissue extensions (e.g., nounced than in other sponge morphologies (Fig. 7). Cup-like sponges
Schönberg and Tapanila, 2006; Schönberg, 2016a, and references commonly have a roughly cylindrical (tubes and barrels) or inverted-
therein), and other anchoring adaptations on their lower half that include cone symmetry (cups) and a small to medium attachment area.
incorporation of fragments and sediment, attachment to or inhabiting Sponges with hollow bodies and wide apical diameters are here com
buried pieces of rock (summary in Schönberg, 2016a). The convex or erect bined as cups and are distinguished from tube-like hollow sponges or
parts of fistular sponges provide the same function as for other erect “narrow cups” with narrow apical diameter, and from barrels with
sponges, as they avoid a build-up sediment on their surfaces and prevent filled bodies and a convex apical depression. Additional example im
occlusion and smothering of important parts of the sponges’ aquiferous ages are provided in Suppl. 4–5.
system. These sponges can further develop a polar morphology to separate Functional context: Cup-like sponges can occur in more flow-
in- and exhalants so that either mostly occur on the elevated parts or on reduced, oxygen- or nutrient-poor environments than other morphol
the main part of the sponge body (e.g., Fry and Fry, 1979; Rützler, 1997; ogies with comparatively low profile (e.g., Schmahl, 1990), because
10
(caption on next page)
11
Fig. 4. Situations in which sponge morphologies should be scored by function, i.e. possibly in a different context than for most traditional approaches. A – This
Chondropsis sp. coats a whip-like structure and should be scored as one-dimensionally erect or simple-erect as it is no longer restricted to the boundary layer. It has
small branches or tubes, but for the overall habit these seem to be of subordinate importance. B – The encrusting cf. Darwinella australiensis commonly coats the
stalked giant sea tulip Pyura spinifera. In this way the sponge attains the overall morphology of the ascidian and should be scored as “stalked” itself as it reaches into
higher levels of the water column. C – The endolithic-bioeroding sponge Cliona caribbaea in “beta” morphology would usually be part of the encrusting sponges, but
in this particular case it inhabits a rounded piece of calcium carbonate and should be scored as simple-massive, with in- and exhalant openings mingling on the same
surface. D – This Plakortis sp. settled on the upper part of an erect structure and has no living tissue closer to the substrate surface. It should be scored as “stalked”
instead of “ball” or “simple-massive”. E – This sponge consists of laminar portions that have no main direction and are robust and densely merged. It cannot inform on
prevailing currents, and due to the compact appearance, it should best be counted as “composite-massive”. F – This Spheciospongia sp. is fistular, even though in this
case it is not buried in the sediment. G – Caulospongia spp. have a central axis and tiers of plate-like, tabular to more convoluted elements. They are three-
dimensionally arranged in the water column and are best scored as erect-branching, unless they become very narrow and dense or develop a longer stalk, in
which case they may function more like a simple-erect or a stalked sponge if the basal part is long. H-I – Ianthella basta is commonly perceived as a fan-shaped, erect-
laminar sponge, but it often forms pronounced tubular structures that would potentially concentrate the exhalant stream, whereas in an erect-laminar sponge this
would not occur. It might thus better be scored as a tubular sponge. J – This Axinella sp. is composed of several laminar parts that are mostly in one plane, and it can
probably still be scored as erect-laminar. If the structure were more complex, but still loosely arranged, this sponge could possibly be scored as three-dimensionally
branching. K – While this sponge mostly consists of laminar parts, they are not aligned in one plane. Due to its central portion, it is partly cup-like, due to the outer
elements partly three-dimensionally branching. Considering the rigid appearance and the orientation that is not governed by flow conditions and seeing the sediment
caught in some of the compartments, this particular sponge should probably be counted as a cup, as composite-massive if it were more densely arranged. L – This
partly-branching, partly-laminar Haliclona sp. settled on the upper parts of a gorgonian and should thus be scored as “stalked”. A, D, F, H-I, J, L – Sponges in − 12 to
− 14 m, Pilbara near Onslow, NW Australia. B, E, K – Photographs from SW Australia by John Turnbull© (2020), with friendly permission. C – Photograph from the
Bahamas by Sven Zea©, with friendly permission (Zea et al., 2014). G – Specimens from the Carnarvon Shelf near Point Cloates, NW Australia, ca. − 60 m.
spatial separation of their in- and exhalants reduces the risk of re- and cups. They may in part be incompletely curled fans or cups with
inhalation of their own wastewater (Bidder, 1923; Bergquist, 1978; Fry, parts missing. In fact, some dictyoceratid cups such as Carteriospongia
1979). The link to nutrient-poor, clear waters may explain that cup-like foliascens can display the whole spectrum between a tabular sponge, cup
sponges with a large proportion of near-horizontal surface can often be and a fan (Fig. 9). While incomplete cups largely function like a wide
photosymbiotic (e.g., Wilkinson, 1988). However, unless they have a high cup, they are not entirely closed, which means that sediments collecting
spongin content (Wulff, 1995), their morphology is not as suitable for within can trickle out or possibly be washed out more easily (Fig. 9E-G).
strong, unpredictable flow regimes, because they can become detached or Examples include e.g.: C. foliascens, Phakellia ventilabrum.
broken. And while damaged sponges or basal pieces that may remain Category 7.3 – Complete, wide cups (Fig. 2A) are basally fully closed
attached to the substrate will often grow back, the dislodged sponge body and entirely hollow and concave sponges in which the apical diameter is
or fragments are less likely to reattach and survive (Wilkinson and usually the largest one. They can be more funnel-, more goblet- or more
Thompson, 1997; Bell and Barnes, 2001a; Gilliam et al., 2009). To some cup-shaped, but they all have a small to medium basal attachment area,
degree cup-like sponges can tolerate sedimentation, because the upper e.g. as a short stem. We need more information about the distribution of
surfaces bear the exhalants. By apically concentrating the exhalant flow, ostiae and oscula in wide cups as they do not always seem to be as clearly
finer sediments that fall onto the concave exhalant areas or into a cup may separated as in other cup-like sponges, or they are not always separated
be washed away, while the coarser particles may collect but still allow in the same way. The exhalants are mostly scattered across the inner,
oxygenation and flow away from the sponge (Fig. 8; Swierts et al., 2018). concave surface of wide cups, but in Carteriospongia foliascens some of
In this as in other cases within the Porifera, coarser materials are usually the oscules may also be found on outer surfaces (Fig. 8B). Some Cym
less stressful or detrimental than fine sediments (Pronzato et al., 1998; bastela spp. were reported with reverse separation, i.e. with inhalants on
Schönberg, 2016b). the concave inner surface and exhalants on the lower convex surface of
Subgroups: Category 7 – Cups (CAAB 10 000910) include tabular or the cup, or with both types of openings on the inner, concave surface
table-like sponges, incomplete and complete cups. Their widest diam (Hooper and Bergquist, 1992; Hall and Hooper, 2019). In such cases,
eter is usually expressed by the apical rim. sediments that collect in the cup cannot effectively be washed out by the
Category 7.1 – Tables (CAAB 10 000920) are very shallow cups exhalant flow (Fig. 9A, C-D), and there would be a high risk of inhaling
that have a near horizontal, flat shape but are not crusts. They have a fine sediments into the aqueous system. Sediments can build up at the
short central stem or small attachment area to hold them in place, but bottom of such cups and cause anoxia and tissue death (Fig. 3I-J in
they are otherwise unattached. Due to this small attachment and Schönberg, 2016b), so that some cup-shaped sponges may develop a
despite having a low profile, they can become dislodged in high en basal or lateral hole and start to function as an incomplete cup (Fig. 9E),
ergy flow regimes, and they would typically inhabit areas with mod or other organisms grow on the concave surface of the sponge, further
erate to strong, but predictable flow patterns. Stagnant water would reducing water exchange (Fig. 9D). Cymbastela spp. have a surface
not be supportive of tabular sponges, as their large upper surface spicule palisade that creates particle-repellent conditions (Schönberg,
could quickly be covered in sediments. Multiple table-like structures 2015b), and many cup-like sponges can shed adhering particles with a
stacked in tiers along an upright axis in a single sponge such as in mucus veil (Fig. 8G, I, K), but overall, hollow cups are not well-suited for
Caulospongia spp. are at the interface between tabular sponges (hori high rates of sedimentation. This is especially true if the sponges are
zontal surfaces) and three-dimensional erect-branching sponges photosymbiotic, such as e.g. the cyanosponges C. foliascens or Cymbas
(increased structure, reach into the water column; Fig. 4G). In this tela spp. (e.g., Wilkinson, 1988; Roberts et al., 2006; Schönberg, 2016b).
case the three-dimensionally distributed body and the erect-branching Many photosynthetic sponges develop morphologies with proportion
function in combination are more important and the sponge should be ally more horizontal surface to maximise the area exposed to light, and
scored instead as erect in three dimensions. Where the branch-like being covered with sediments would reduce the primary production by
structure is very close to the central axis and the sponge is long and shading. Therefore, these sponges are usually less abundant at turbid
slim, it can instead be scored as simple-erect (e.g. as in Fig. 4A). Ex sites with high sedimentation rates of fine sediment, and more common
amples for simple tabular sponges include e.g.: flat Cymbastela spp. in at clear-water, more nutrient-poor sites with coarser sediments (Wil
the Demospongiae, and Bathydorus spp. and Docosaccus spp. in the kinson, 1988; Wilkinson and Cheshire, 1989; Wilkinson and Evans,
Hexactinellidae. 1989). Examples for complete, wide cups include e.g.: Axinella infundi
Category 7.2 – Incomplete cups or curled fans (CAAB 10 000918) are buliformis, Cliona patera (or it can be stalked), Ircinia campana, Echino
an intermediate form between erect-laminar sponges and cups or tables dictyum mesenterinum. Some species can produce cups stacked inside of
12
Fig. 5. The simple-massive sponge Spongia (Spongia) officinalis in the Mediterranean as an example for mixed or patchier oscular grouping that can be more
concentrated at the apex of the sponges (A-D), compared to the here functionally simple-massive sponge Cliothosa delitrix with relatively evenly mixed in- and
exhalants (E) and the barrel Xestospongia testudinaria, in which ostiae and oscules are on different body surfaces (inhalant phase: F, exhalant phase: G). The
S. officinalis individuals are not exactly to scale, but the distribution and location of the oscules, their more pronounced oscular collars, their diameter and the more
vertical growth of the sponge in D suggests that this site had the lowest flow and was likely the most oligotrophic, requiring this sponge to separate in- and exhalants
more clearly than in the other specimens and to reach higher into the water column. Oscular grouping results in spatially combining the flow of separate exhalant
openings, creating a stronger jet that carries wastewater further way from the sponge (Fry, 1979). In C. delitrix in − 13 m at Looe Key, Florida exhalants are distributed
across the entire surface, but in this case the water is predominantly exhaled from the top of the sponge, creating a morphologically less clearly defined and more
behaviourally realised separation (E). In X. testudinaria in − 4 to − 5 m at Orpheus Island, Great Barrier Reef a clear separation exists between lateral inhalants on the
outer surface (F) and apical, grouped oscules producing a single, exhalant stream spatially separated from the inhalants (G). A – Photograph by Roberto Pronzato©,
with friendly permission. B-D – Photographs by Thanos Dailianis©, with friendly permission. The passage of the water was made visible by the use of fluorescein dye
in E-G.
13
cups (e.g. Cymbastela marshae) or spiral cups (Carteriospongia sp. LG 1, p.

100 in Goudie et al., 2013) – these still function as complete cups.
Category 8 – Narrow cups or tube-like forms (CAAB 10 000926), i.e.
tubes and chimneys (CAAB 10 000911; Fig. 2B) and sack- or amphora-like
forms (CAAB 10 000927; Fig. 2C), are extreme forms of cup-like sponges.
In cross section they are hollow along most of their body. Proper tubes
have apical openings that have a diameter similar to the tube or body
diameter, while sack- or amphora-like forms are barrel-shaped, but hollow
sponges, with apical openings that are smaller than the maximum spon
ge diameter. In both morphologies the exhalant stream is strongly
bundled by a single exhalant opening, situated apically. Thereby, narrow
cups are best adapted to and protected from moderate sedimentation
pressure (Krautter, 1998; Bell, 2004) and have never been reported to
accumulate sediments in their lumens. Nevertheless, we need more data to
better understand the ecological role of tube-shaped sponges. As in erect
sponges, most of their surfaces are vertical and do not collect significant
amounts of sediments. Nevertheless, they are usually reported from clear
waters (Suppl. 2), and the tubular Aplysina aerophoba grew faster when
sedimentation was excluded (Wilkinson and Vacelet, 1979). If one sponge
individuum is formed by several tube-like structures arranged in a group,
it may function more like an erect-branching or an erect-palmate sponge
when in clear-water environments, or more like a battery of narrow cups if
sedimentation is high. However, the tubular shape is such a specialised
morphology that it may usually be best to score it as tube-like sponge, as
long as the oscular opening is similar to or smaller than the diameter of
this part of the sponge. Some sponges such as Ianthella basta form erect-
laminar morphologies when they are small, but can grow into large
tube systems and should then be counted under “narrow cups” (Fig. 2B,
4H-I). The Atlanto-Caribbean has many examples of tubular sponges and
only few are known from Australia: Callyspongia (Cladochalina) aculeata,
Agelas tubulata, Aplysina fistularis, Liosina paradoxa, Pipestela candelabra,
Echinochalina (Protophlitaspongia) isaaci. The glass sponge Euplectella as
pergillum would be a good example from the Hexactinellida, even though
the apical exhalant opening is covered by a delicate spicule mesh. Ex
amples for amphora-like demosponges include e.g.: Mycale (Arenochalina)
laxissima, Theonella swinhoei, glass sponges such as Rossella spp., Anox
ycalyx (Scolymastra) joubini, wide specimens of E. aspergillum, and
calcareous sponges such as Sycon spp.
Category 9 – Barrels (CAAB 10 000907; Fig. 2C) embody a special
form of cup-like sponges. While they have a massive appearance due to
their overall shape and tissue distribution that fills most of their body,
their main function is driven by the cup-like separation of in- and ex
halants (Fig. 5E-F). The exhalants are located on a concave apical
portion that creates a similar, bundled exhalant stream as in narrow
cups, but here the jet is slimmer than the apical opening and less well
defined than in tubular forms. The inhalants are situated on the outer,
lateral surface. The sponges can be more conical, more barrel-shaped or
more globular, but often quite large. They can commonly tolerate
reduced flow and high rates of sediment deposition, and fine sediments.
Some barrels are photosymbiotic cyanosponges. Classic examples for
barrels are e.g. larger Xestospongia spp. (Fig. 2B, 8, 5F-G), Ircinia strobi
lina, Spheciospongia vesparium and Geodia neptuni.
3.1.4. Sponges functioning as erect forms (CAAB 10 000913; Fig. 3)

Definition: Erect sponges have a very small attachment area; their
main body is in the water column, and in considerable distance from the
substrate and the boundary layer. These sponges are predominantly Fig. 6. Xenospongia patelliformis is an unattached sponge highly adapted to
sandy environments. A – Sideview: When dredged up and without context,
vertical and have minimised their horizontal surface areas. Oscules and
larger individuals can easily be mistaken for a cup. B – However, the sponge
ostiae are not usually as clearly separated as in the cups (Fry, 1979).
rests unattached on the substrate convex side up. Note that the sponge is quite
They can be situated on vertical surfaces, on branch apices or in a line
conical and thus not prone to burial. The arrow points to the large apical
along a ridge or the top of a branch, However, they can be mostly osculum. C – The lower side contains densely embedded particles to weigh the
divided between the two prevailing surfaces on vertically flattened, fan- sponge down. D-E – A smaller individual is flat and disc-shaped, D – upper
shaped sponges, with the exhalants mostly facing downstream. Further surface, E – lower surface (D-E are at 1.5x the size of A-C). The sponges were
examples for erect sponges are depicted in Suppl. 4–5. sampled on sandy bottom in − 66 m off Point Cloates, Carnarvon Shelf in NW
Functional context: Due to their height and small attachment area, Australia (Schönberg and Fromont, 2012).
erect sponges can be vulnerable to fragmentation, detachment and
14
Fig. 7. Examples of the spatial distribution of

in- and exhalants in different growth forms of
sponges. A-D have fully mixed in- and
exhalant openings and rely on external cur
rents to carry off used exhaled water and
provide enough flux of fresh oxygenated and
nutritious water. In E, oscules are all located
apically but still on the same surface as the
inhalants, and in F they are grouped in
patches to better bundle exhalant jets. In G
entry and exit points are situated on the tops
of fistules, thus somewhat better separated,
despite being on the same plane. H-L are ex
amples for cup-like sponges that are assumed
to take up water through pores on their lateral
sides and eject it from concave surfaces on the
inside of the “cup”. Depending on the oscule
and “cup” diameters, the exhalant flow can be
bundled as a strong jet, carrying the waste
water well away from the sponge, even at low
ambient flow speeds. A – Encrusting Placos
pherastra micraster, Bahamas (J. Pawlik; see
taxonomic remarks on Zea et al., 2014 re
genus name). B – Simple-massive Hyrtios cav
ernosus, Bahamas (S. Zea). C – Erect-branching
Aplysina archeri, Bonaire (J. Pawlik). D –
Creeping Clathria (Thalysias) virgultosa,
Bahamas (S. Zea). E – Creeping Neopetrosia
subtriangularis, Bahamas (S. Zea). F – Simple-
massive Asteropous niger, Bahamas (S. Zea).
G – Fistulate Siphonodictyon coralliphagum,
Bahamas (S. Zea). H – Globular Cinachyrella
kuekenthali, Bahamas (S. Zea). I – Barrel or
cup-like Verongula reiswigi, Martinique (J.
Pawlik). J – Here incomplete cup Ircinia
campana, Curaçao (J. Pawlik). K – Cup Cri
brochalina vasculum, Bahamas (J. Pawlik). L –
Tubular Aplysina cauliformis, Bahamas (S.
Zea). Photographs from Zea et al. (2014),
creative commons, individual photographers
as indicated in brackets.
15
Fig. 8. Sediment deposition in cup-like sponges. A-B – Barrel-shaped Xestospongia testudinaria in 12–14 m at Onslow on the Pilbara coast, NW Australia. The sponges
discharge an exhalation stream from the upper and inner, concave surface. While this habitat was characterized by fine, mud-like sediment, a high turbidity and high
sedimentation rates, the grains remaining in the concave parts of the barrels were coarse, the exhalant water having washed out the fine material.
removal due to strong flow, waves or storm surges, unless they have a are strong bioindicators for laminar currents, in which they arrange
high spongin content that makes them flexible (e.g., Jackson, 1979; themselves at right angle to the main flow direction.
Wulff, 1995; Fig. 10). However, some branching sponges have a high Category 11.1 – Erect-laminar sponges (CAAB 10 000912; often also
survival rate after fragmentation and can quickly re-attach and regen called flabellate or foliaceous sponges, Suppl. 1) have erect morphologies
erate (Wulff, 1985, 1991, 2006a), which can result in similar before- with a simple, vertically flattened body and a comparatively small attach
after-storm counts. Disregarding acute events such as storms, erect ment area and include forms such as fans, blades and spatulas. The blade
sponges commonly occur in habitats with benign or predictable flow can have short fissures or a few holes, but the overall body form is mostly
regimes and become simpler with decreasing exposure and increasing intact. Erect-laminar sponges of significant height are commonly flexible
sedimentation (Abraham, 2001; Bell et al., 2002a; Lawler and Osborn, and have a high spongin content, and they bend when larger flow speeds
2008). Mixing of the water column and renewal of nutrients and oxygen are reached, e.g. in strong tidal currents (Fig. 10A; Schönberg and Fromont,
is lower near the substrate surface (Mendola et al., 2008), and erect 2012). They stand at right angle to prevailing directional flow (de Lau
sponges reach up into the water column to maximise feeding by bringing benfels, 1936; McDonald et al., 2003; Schönberg and Fromont, 2012),
inhalant openings into water away from the boundary layer, avoiding thereby maximizing the yield of nutrients. In places such as channels, where
the more depleted layers close to the substrate, and enhancing ventila the currents predominantly proceed in only one direction, the in- and ex
tion and waste removal (Bidder, 1923; Jackson, 1979; Jones, 1994). halants can become mostly separated, i.e. most of the inhalants would face
Sponges situated at a higher level of the water column grow faster than into the flow, and most of the exhalants would be on the downstream side of
those closer to the substrate surface (McLean and Lasker, 2013). With the sponge’s blade (de Laubenfels, 1936). Where this occurs, the most
the exception of balls, sponges develop larger heights at sites with less efficient separation of in- and exhaled water is achieved (Bidder, 1923;
water movement than at more exposed sites (Lawler and Osborn, 2008). Bergquist, 1978). De Laubenfels (1936) observed that many erect-laminar
Erect morphologies are more resistant to sediment deposition, clogging sponges do not change their morphology to colonise other flow regimes,
and smothering as their predominantly vertical surfaces and some apical but only occur in laminar flow. Examples include e.g.: Ianthella flabelliformis
arrangement of oscules prevent particle build-up (Bell, 2004; Divine, (Fig. 10A), Stylissa flabelliformis, Clathria (Thalysias) costifera and C. (T.)
2011). Erect sponges can occur in highly turbid habitats with high levels placenta. If laminar sponges lose their two-dimensionality by having mul
of suspended particles and high sedimentation rates, while most of the tiple blades arranged in different directions, they no longer reflect laminar
other morphologies do not tolerate such conditions as well (Lawler and flow conditions and can become functionally more like composite-massives
Osborn, 2008). if densely merged or erect-branching if loosely arranged (Fig. 4J-K).
Subgroups: Category 10 – One-dimensional or simple-erect sponges Category 11.2 – Erect-palmate sponges (CAAB 10 000914; Fig. 3A,
(CAAB 10 000916) are significantly higher than wide and do not branch or 10B) are sponges with branches oriented in one plane like fingers on an
only to an insignificant amount. These are whip-like or columnar sponges open hand. The branches can be and are often flattened, but do not have to
(not tubular structures such as fistules). In cross section they are solid. be. Palmate sponges very much function like the other two-dimensional
Literature providing information about the environmental conditions sponges, except that they experience less drag. Many palmate sponges
simple-erect sponges occur in is scarce (Suppl. 2), but high sedimentation also have a high spongin content and bend in the currents, but they
pressure appears to induce branch reduction in three-dimensionally commonly have a more rigid consistency, when spongin is reinforced with
branching sponges (Bell et al., 2002a), and simple-erect sponges are inorganic spicules. Examples include e.g.: Trikentrion flabelliforme, Ectyo
sedimentation-tolerant. Whips and rope-like sponges often contain much plasia tabula, Reniochalina stalagmitis, Clathria (Thalysias) major, C. (T.)
spongin and are flexible, while columnar sponges are usually more reliant spinifera and Ernstilla lacunosa (Fig. 10B).
on their inorganic skeleton. This would mean that whips can likely tolerate Category 11.3 – Erect-reticulate (CAAB 10 000929; Fig. 10C)
high energy environments, but columns would rather be found in less sponges are vertical meshes in one plane, i.e. when an erect-laminar
exposed situations with reduced flow and in that respect may function sponge has many holes or when the sponge consists of branches that
more like simple-massive sponges. However, both reach up high into the reconnect to form a flat, vertical lattice. They function like the other
water column, and the ambient nutrient conditions may thus be limited. two-dimensional sponges, but due to their composition of inorganic and
Examples include single branches of usually three-dimensionally erect- organic skeleton they are often firmer and thus rely on the gaps to reduce
branching species e.g.: rope sponges such as Aplysina fulva, Haliclona the drag caused by currents. Examples include e.g.: Axinella australiensis,
koremella, Clathria (Thalysias) procera. Iophon minor, Echinodictyum pulchrum, Clathria (Clathria) hjorti, C. (C.)
Category 11 – Two-dimensionally erect sponges (CAAB 10 000928; multipes, Clathria (Thalysias) coppingeri (Fig. 10C).
Fig. 3A, 10) are erect-laminar or fan-shaped, erect-palmate or branching Category 12 – In three-dimensionally, erect-branching sponges
in one plane, and erect-reticulate or erect meshes in one plane. All three (CAAB 10 000914; Fig. 3B) branches are longer than wide and arranged
16
Fig. 9. Examples for different morphological expressions in the same sponge species, ranging from cup- to fan-like forms in Carteriospongia foliascens in − 1 to − 3 m in
the Palm Island Group, central Great Barrier Reef. A-D – Complete cups, partially with additional structure (B-C) and commonly collecting sediments that cannot
easily be washed out (A, C) so that they sometimes become substrate for other organisms (D). Please note the widely spaced, small oscules predominantly on the rim
and on the inside of the cup in A (arrows). Ex- and inhalants are not completely separated between inner and outer surfaces in C. foliascens (B, arrows). E-G – Slightly
incomplete cups may have resulted from necrosis after sediment accumulation, or from spongivory or other damage. H-K – Intermediate stages between incomplete
cups and erect-laminar forms. L-N – Erect-laminar morphologies. O – A composite-laminar form in three dimensions functioning more like an erect-branching than a
fan-shaped sponge. P – A fan horizontal to the substrate can be scored as tabulate. Arrows in G, I and K denote mucus veils in sponges that slough off material to clean
their surfaces.
17
fascicularly (bush-like, merging out from a common base at the sub

strate) or arborescently (tree-like, merging out from a common, short
stem that can bear in- and exhalants, and having a more complex
branching pattern). Oscules and ostiae are mostly mixed and scattered
across the sponges’ surfaces and can reach down to the short stem, but in
some species the oscules can be arranged in lines along the branches
(Fry, 1979). This branching pattern may most commonly develop as a
response to reduced water mixing and limited access to nutrients near
the substrate, and the predominant sponges stretch into the water col
umn to reach enhanced flow and nutrient conditions. In erect-branching
sponges their number of secondary branching and total branch number
increases with flow (Lawler and Osborn, 2008). Due to their more fragile
morphology, three-dimensionally branching sponges are usually
excluded from areas with strong and turbulent flow and only start in at
deeper depths, where those flow regimes become more benign (e.g., Bell
and Barnes, 2000a). However, they can be more resistant to disease, due
to slower spread within an infected branching sponge relative to an
infected massive or encrusting sponge, or recover faster after mortality
events due to high tolerance to fragmentation and fast regrowth rates
and may at least temporarily become dominant after disturbance (Wulff,
2006a, 2006b, 2006c). Groups or clusters of fan-like or tube-like com
posite structures can occasionally be scored as erect-branching if their
function within the given environment is more strongly governed by the
erect growth, sediment and food conditions than by flow conditions. If
such clusters become very dense and well-merged, they may be scored as
composite-massive sponges. Where branching sponges have settled on
an erect structure in considerable distance from and without connection
to the substrate, they should be scored as stalked (Fig. 4L). Examples
include e.g.: Pararhaphoxya sinclairi, Raspailia (Raspaxilla) topsenti.
Category 13 – Stalked-erect sponges (CAAB 10 000906; Fig. 3C)
represent a very specialised morphology. They have a clear separation of
a basal stalk-like portion that does not normally contain any obvious
ostiae or oscules, and an apical part that represents the main body with
all the functional parts. Short stems differ from stalks in that the former
can contain functional parts. The elevated body can exhibit different
forms and can be globular or even cup-like, as long as it is clearly
removed from the substrate and the boundary layer by a largely “inac
tive” stalk, which can mostly consist of spongin or of inorganic skeleton
– or it can be a foreign object the sponge settled on (Fig. 4D, L). This is
one of the most extreme adaptations to poor nutrient conditions, and
many deep-sea sponges display this morphology as this environment is
depauperate of the typical food sources of shallow water environments
(e.g., Leinfelder et al., 1996; Krautter, 1998). Stalked sponges can occur
in areas with different substrates, and if there is fine sediment, the stalk
is also a good means to remove the sponge from the deleterious mud.
Stalked glass sponges often turn their convex side with the inhalant
pores into the current and the wide concave side with the exhalants
points downstream so that the wastewater is more easily carried away
(Bergquist, 1978; Tabachnick, 1991; Janussen pers. comm.). Bidder
(1923) said about such hexactinellid sponges: “In the great depths where
they live, an unchanging current sweeps slowly from the poles to the
equator. They have but to spread a net across it. […] Such an organism
becomes a mere living screen between the used half of the universe and Fig. 10. Examples of two-dimensionally erect sponges typical for habitats with
the unused half.” Some morphologies can be quite complex and may strong tidal currents in NW Australia. A – Ianthella cf. flabelliformis (light blue-
communicate between branching or palmate and stalked morphologies, green blade), and B – the palmate Ernstilla lacunosa in − 12 to − 14 m at Onslow.
depending how far more complex structures reach down the stalk, e.g. Both species have an exclusively organic skeleton (spongin). Note that the other
Chonelasma spp. Examples for demosponges include e.g.: Tethycometes branching organisms in this habitat were also usually two-dimensional and
radicosa, Podospongia virga, Stylocordyla chupachups, Rhizaxinella spp., arranged at right angle to the predominant flow direction created by tidal
Clathria (Thalysias) fusterna, and e.g. Hyalonema spp., Bolosoma spp., currents in the area. The orange branching sponges would be either Axos or
Caulophacus spp. for glass sponges. Clathria spp., sponges with inorganic and organic skeleton, but with a high
Category 14 – Carnivorous sponges (CAAB 10 000930; Fig. 3D-E) content of the latter. C – A benchtop photograph of the erect-reticulate Clathria
(Thalysias) coppingeri with spicular skeleton and a high spongin content, from
mostly occur in nutrient-limited deep water or occasionally in caves and
− 24 m at southeast Montgomery Reef, Kimberley, northern Australia. (For
are the most extreme adaptation to food limitation in sponges (Hajdu and
interpretation of the references to colour in this figure legend, the reader is
Vacelet, 2002). Their habitats are generally unsuitable for filter feeding or referred to the web version of this article.)
so oligotrophic that these sponges have reduced or abandoned their
aquiferous system and instead rely on velcro-like surfaces with protruding
18
Table 3
Dominant sponge morphologies in relation to prevailing environmental conditions and the strongest environmental drivers. All major environmental factors below covary to some extent (Jackson, 1979), and they change
C.H.L. Schönberg
along the same axis downwards in the table. The observations for sponge functions relate to horizontal substrate and are here supported by a few key publications. The terminology for morphologies follows the present
concept. Details and further references are provided in Suppl. 2. In situ examples are provided by Figs. 1-3.
Environmental factor Expected predominant sponge morphologies Ecological implications
Hydrodynamic regime (see e.g. Wulff, 2006a; Schönberg and Fromont, 2012)
Strong, turbulent flow Firmly attached encrusting, simple-massive, and some ball-shaped sponges Drag, acceleration and lift can break and dislodge any sponge with high profile, delicate consistency
(Fig. 1A-C), with comparatively low profile, large attachment area and relatively small size, at and weak attachment. Having a small, compact size, a firmer tissue : skeleton composition and a
times reinforced by a high skeleton content; oscules may be comparatively small. low profile is thus a survival strategy. The strong flow regime and good mixing do not require a
clear separation of in- and exhalant openings, and oscules can remain small due to good mixing of
the water column.
Strong, laminar flow Often flexible, two-dimensionally erect sponges (Fig. 3A) with a high spongin content, as well as Erect forms are thought to extend vertically into faster flow regimes to gain better access to food
some ridge-like simple-massive sponges dominate (Fig. 3B); they will orient themselves at right and to eliminate waste products. Flat shapes at right angle to the flow optimize this effect, creating
angle to the flow. Fistular sponges can also be common in laminar flow (Fig. 1D). eddies. When having a small attachment : body area, flexibility safeguards against dislodgement.
The peak flow regime does not require a clear separation of in- and exhalants, but some sponges
exhibit a separation by having most exhalants placed at the surface facing prevailing downstream
currents or on apical ridges.
Moderate, predictable flow Morphologies may be diverse but may increasingly include erect components apart from Erect forms are thought to escape the flow-reduced boundary layer by reaching into faster flow
morphological complexity. Cup-like, erect and massive sponges are usually common in medium to regimes to gain better access to food and to eliminate waste products, which encrusting sponges
low flow, as well as a more pronounced separation of in- and exhalants. Encrusting forms become cannot, unless they develop erect structures such as fistules, or they grow on vertical surfaces. With
uncommon. With flow reduction oscular diameter and erect specimen height increase (Fig. 5A-D), diminishing flow sponges separate in- and exhalant openings to reduce the risk of re-inhaling food-
but balls become smaller or flatter, and branch number, branch width and branching complexity and oxygen-depleted water and waste products (esp. in cup-like morphologies). Moreover, with
are reduced in erect sponges. reduced flow sedimentation increases, and horizontal body surfaces are of disadvantage, and large,
apical exhalant structures of advantage to concentrate the exhalant jet and to blow sediments away.
Low-flow, stagnant or nutrient-poor Erect, and especially stalked forms predominate (Fig. 3C), or carnivorous sponges as an extreme ( Erect structures extend the reach into flow regimes beyond the boundary layer to gain better access
conditions, sediment fine and soft Fig. 3D-E). Otherwise sponges may develop erect structures on their surfaces. In stalked glass to food and oxygen, and to eliminate waste products that are carried away by remaining currents.
where present sponges, the body often has a concave side (facing downstream) and a convex side (facing into the Stalked forms represent an extreme by significantly separating and elevating the bulk of their body
prevailing current; Fig. 3C). mass from the substrate and the boundary layer. This also removes the body from soft, fine
sediments that are most deleterious to sponges. Exhalants may be placed on surfaces facing
downstream to maximize the removal of the exhaled water. Where food supply becomes limiting to
19
filter-feeding, carnivorous sponges occur.
Substrate type (see e.g. Schönberg, 2016a, 2016b)
Prevailing rocky, hard bottom All sponge morphologies can be found on rock, but crusts and simple-massive sponges usually Most sponges can only settle on firm substrate, and bedrock would be the safest. If the habitat is
dominate (Fig. 1A-B). If the hard substrate is calcium carbonate, endolithic-bioeroding sponges characterised by bare rock, it is likely an exposed site where sediments cannot easily settle. In such
may be abundant (Fig. 4A). an environment, low-relief morphologies with a large attachment area and forms that reduce risk of
scouring will prevail (see above).
Prevailing sandy bottom Endopsammic, fistular Sandy ground is suggestive of a milder flow regime than for rocky bottom but offers less suitable
(Fig. 1C) or endolithic-bioeroding sponges will be dominant, and some creeping-ramose sponges substrate to colonise. Sponge larvae often settle on small stones, shells or other fragments, and can
may occur. All of these are likely to have oscules in apical positions, most typically on elevated, later anchor themselves within the substrate by agglutinating more such material, or by including
fistular structures. sand and particles into their tissues and by growing root-like extensions. Sand may shift and move
and may cover organisms living in this area, and fistule-like structures will prevent smothering.
Prevailing muddy bottom Fistular and erect sponges are most dominant (Fig. 1C, 3). With even less water movement, fine sediment will settle out, which is overall more harmful to
sponges than coarse sediment and may clog the aquiferous system after being inhaled and can cause
anoxia and necrosis where tissue becomes covered for longer time. In such an environment all
sponges will have erect or convex components that emerge from the mud (fistules) or elevate them
above the fine sediments (various erect forms, incl. stalks).
Ecological Indicators 129 (2021) 107806

Water clarity, sedimentation (e.g. Wilkinson, 1988; Wilkinson and Cheshire, 1989; Wilkinson and Evans, 1989)
Clear, nutrient-poor water Many sponge morphologies can occur in clear water, but cup-like morphologies may be most Clear water relates to a reduced nutrient load, which requires sponges to separate their in- and
common (Fig. 2A). Crusts may also prevail exhalant streams to maximize the feeding success, or they supplement their nutrition by
(Fig. 1A). photosymbiosis, and many photosymbiotic sponges are wide cups with much horizontal surface
exposed to light. Crusts can survive without becoming smothered by sediment.
Turbid water Globular (Fig. 1C), erect-laminar, erect-palmate (Fig. 3A), and erect-branching sponges will be Turbid water suggests reduced flow and fine sediments, which selects for erect morphologies to
common (Fig. 3B), as well as some cup-like sponges (Fig. 2B). reduce the amount of surface area on which sediment can settle. Cup-like morphologies commonly
have exhalants on their upper surfaces, which reduces the risk of inhaling sediment (e.g. barrels).
High sedimentation rate Fistular sponges will occur (Fig. 1D). Sponges with otherwise unornamented surfaces may develop The best-adapted sponges will be those that can live buried in the sediment and that have fistules
erect or convex portions. Barrels and tubular sponges can occur (Fig. 2B). Crusts may survive on and erect or convex structures that emerge from the substrate. As above, sponges that can keep their
vertical surfaces. upper surfaces clean by washing sediments away with a strong apical exhalant stream are also well
adapted.
Fig. 11. Proposed distribution of different sponge morphologies in a continuum of different environmental conditions according to the present understanding of their
functions as summarised in Table 3 (see also Suppl. 2).
spicules that trap e.g. little arthropods that are then engulfed by sponge community structure, its function, ecosystem health and environmental
tissue and digested (Vacelet and Boury-Esnault, 1995). The morphologies conditions (e.g., Bremner et al., 2003; Petchey and Gaston, 2006; Saito
of carnivorous sponges can be very variable among taxa but are often et al., 2015; Zawada et al., 2019). The proposed sponge classification
delicate and mostly stalked or erect-branching in different patterns, with scheme caters for the same outcome: morphologic and functional diversity
fine, ray-like branchelets extending comb- or bottle brush-like from their can be used as a proxy for taxonomic community diversity, even if based
axes for prey capture (e.g., Vacelet, 2006, 2007, 2008; Lee et al., 2012; only on imagery (Lauder, 1990; Bell and Barnes, 2001b; 2002; Bell,
Vacelet, 2020). Carnivorous sponges may be confused with other erect 2007a; Giribet, 2015; Hadi et al., 2015; Gerovasileiou and Voultsiadou,
sponge morphologies (palmate, branching, stalked). This may not much 2016). In addition, the scoring structure is designed to explain dominant
change the outcome of the interpretation of environmental conditions, functional traits of the sponges, which can in turn inform on disturbance
however, as long as these extreme forms of erect morphologies are un or functional shifts, as has been done in similar benthic groups (e.g.,
derstood as an adaptation to oligotrophy or reduced flow. Carnivorous Alvarez-Filip et al., 2011; Álvarez-Noriega et al., 2016). Moreover,
sponges are here listed as a separate morphology, because they represent strongly predominant morphologies can act as surrogates for prevailing
the strongest deviation from the basic physiological functions in sponges, environmental conditions (Table 3, Suppl. 1). Similar insights have earlier
but they may respond to subtle ambient flow conditions with two- and been realised and applied for very different benthic assemblages and taxa,
three-dimensionality as do other erect sponges. Carnivorous sponges such e.g. for corals (e.g., Denis et al., 2017), polychaetes (e.g., Bonsdorff and
as Abyssocladia spp., Cladorhiza spp. and Chondrocladia spp. belong into Pearson, 1999), fishes (e.g., Bellwood et al., 2019) and macroalgae (e.g.,
the family Cladorhizidae (Fig. 3D-E). Balata et al. 2011), and sponge surveys based on the present scheme can
yield comparable data (e.g., Bell et al., 2017). As long as a standardised
system is used, such data can provide a wide range of spatial and temporal
3.2. Application of the sponge classification scheme based on functional
context and can fit into the CATAMI classification system (http://catami.
morphologies
github.io/) and other monitoring or classification systems such as e.g.
proposed by Gutt (2007) or Makowski et al. (2009).
The proposed classification scheme will enable science and manage
According to the present observations, hydrodynamic and sediment
ment to quantify sponges widely and consistently for environmental sur
conditions appear to be the strongest selective forces for certain sponge
veys of the marine benthos. Traditionally, surveys that aim to detect
morphologies (Fig. 11) and may have the most impact on sponge func
differences or changes in biologic communities relied on the quantifica
tions, which is in agreement with earlier results (e.g., Carballo et al.,
tion of biodiversity via taxonomy or by assessing trophic guilds (e.g.,
1996; 2008). With the exception of carnivorous sponges, all physiolog
Bremner et al., 2003). However, limitations to resources or expertise or by
ical functions in sponges rely on the pumping of water through their
hazardous environments can prevent easy access to such information.
aquiferous system: the inhalant water carries food, oxygen and sperm
Instead, recent environmental surveys increasingly include other obser
into the sponges, the exhalant water releases waste and sexual products
vations accessed with different means. They look into the link between
(e.g., Reiswig, 1970; Fry, 1979; Weissenfels, 1992; Nickel et al., 2006;
biota and their ecosystems and generating quantitative data about the
20
Fig. 12. Common interrelationships between sponge morphologies – many forms can express intermediate shapes. Arrows connect morphologies that are not
depicted next to each other but can still merge into each other or develop intermediate shapes. From top to bottom and left to right: 1 – Functional crusts (crusts,
endolithic bioeroding, creeping, insinuating), 2 – functional massives (simple, globular, composite, fistular), 3 – functional cups (table, incomplete, complete-
infundibuliform, complete-vasiform, tubular, amphorate, barrel), 4 – functional erect forms (1D: whip, column, 2D: spatulate, flabellate, flabellate to palmate,
palmate, 3D: thickly branching, thinly branching; stalked; carnivorous). Within the cup-like forms and within the 1D to 2D erect forms all hybrid forms are possible.
Bell, 2007b; Schläppy et al., 2007). Water movement is thus vitally specialists that tolerate burial in sediments by stretching parts of their
necessary to bring new supplies to the sessile organisms and to carry bodies vertically into the water column or develop convex, knuckle-
away the expelled materials. At the same time, sediments may exert a shaped portions, parts that remain free of sediment deposition (Bell
risk of occlusion and clogging of the aquiferous system, especially finer and Barnes, 2000a; Fig. 1D). In this way, sponge morphologies and
sediments (Schönberg, 2016b). In sponges, the hydrodynamic environ environmental conditions are clearly linked, and ecological information
ment will therefore impact on almost every aspect of life. Where ambient relates most often to the hydrodynamic conditions.
water movement becomes too violent or turbulent, sponge morpholog There are some constraints to the present scheme, however, and the
ical diversity becomes reduced due to the damaging effect on the more functional context is always very important. The surrogate information
fragile growth forms, and sponges with a large attachment area such as about environmental conditions here discussed only becomes available
crusts and massive forms will be favoured (Bell and Barnes, 2000a; from sponges growing on horizontal surfaces. Where they grow on
Fig. 1A-C). In moderate flow with less mixing, separation of in- and vertical surfaces or underneath ledges, they experience other flow re
exhalants will occur (Figs. 2, 5, 7). In environments characterised by gimes than their morphologic equals on open horizontal ground. On
finer sediments, erect forms dominate that stretch into the water col vertical and inverted surfaces they would also escape sediment deposi
umn, either to reach fresh supplies, or to lower the proportion of hori tion, and where they grow underneath stones, they cannot attain larger
zontal tissue area to minimise effects of sedimentation (Bell and Barnes, and more complicated growth forms. Sponges in such microhabitats are
2000a; Fig. 3). Two-dimensionally erect sponges are a distinctive group also less recognisable, less visible or even invisible on imagery. Apart
to indicate laminar flow (Lawler and Osborn, 2008; Fig. 3A). Carnivo from this, encrusting sponges have been identified as superior space
rous sponges are a very specialised group that no longer relies on the competitors (Jackson, 1979; Aerts and van Soest, 1997). However, it has
aquiferous system, and their occurrence suggests food limitation also been argued that at sites with much live cover and high pressure of
(Fig. 3D-E). Flow conditions will have further, indirect impacts on space competition, sponges with small attachment area or fast-growing
sponges, e.g. by affecting the presence and quality of sediments, species such as commonly found in creeping forms may emerge in favour
turbidity and sedimentation. Fistular, endopsammic sponges are of other morphologies (Hadi et al., 2015) – which is another theory that
21
Fig. 13. Assessment of underwater imagery in turbid environments can be very difficult either through lack of contrast or by backscatter of light reflecting off
suspended particles (A, B; here forward image capture, rather than downwards, in − 10 to − 15 m, Onslow, NW Australia). Image enhancement can bring out more
details (C, D) and allows scoring of more forms than apparent on A-B; forms indicated above each sponge: C-b – barrel (Xestospongia testudinaria), C-cmp – complete
cup, C-t – tubular sponge (Ianthella basta), E – erect (in this case it is likely palmate, but cannot conclusively be evaluated as it is mostly cut off), E-lam – two-
dimensionally erect-laminar (Ianthella sp.), E-pal – two-dimensionally erect-palmate (cf. Axos sp.), E-r – two-dimensionally reticulate-erect (cf. Echinodictyum
pulchrum), M− c – composite-massive, M− s – simple-massive. Digital enhancement can render underwater imagery quite grainy, and it is at the expense of an
increased effort. Examples for scoring from images that were obtained with the camera pointing downwards are given in Suppl. 6.
may require more evidence. Environmentally driven selection for + Assessing sponge communities through imagery can significantly
certain morphologies will be more strongly expressed and will generate shift costs from fieldwork to the office and time expense from sam
clearer form dominances when the drivers are few and strong, with pling and species analyses to data evaluation (Bell, 2007a; Althaus
visible effects not being diluted by antagonistic factors (Jackson, 1979). et al., 2015; Bell et al., 2017). Thereby larger areas can be surveyed
It also needs to be understood that the proposed sponge morphol in less time than by physical collection, thus producing larger, more
ogies are not static, and not always immediately obvious. There are complete and more generally applicable datasets. This is especially
morphologic continua and intermediate forms that can make unam important for taxa that are as patchily distributed as sponges (e.g.,
biguous scoring difficult (Fig. 12). Also, the ecological context can Barnes et al., 2006, 2013).
change the functional setting for each morphology (Fig. 4), as was + The proposed approach readily fits into published and tried Austra
explained above during the definition of the functional morphologies. lian classification schemes including other biota and geomorpho
Moreover, the factors here considered as selective forces for the sponge logical features (Last et al., 2010; Althaus et al., 2015), and can be
morphologies are acting at the survival or growth level, not so much at fitted into non-Australian schemes (e.g. Gutt, 2007; Makowski et al.,
the level of settlement and establishment as has also been discussed by 2009). These schemes are suitable for marine habitats globally.
e.g. Jackson (1979). These early phases of community formation and + Monitoring programs often rely on simple approaches in accordance
maintenance also play a role and may further complicate the situation with resources and means, and they commonly depend on assistance
and can lead to temporal successions of morphologies. Jackson (1979) by non-experts. The simple nature and the detailed images and ex
proposed that in such a succession, disturbance creates newly available planations for the present scheme remove the necessity of specialist
substrate, which should first be colonised by creeping and encrusting participation and allow non-expert involvement, e.g. citizen scien
forms. Under good conditions and reduced disturbance, the community tists, as long as they can recognise sponges and distinguish them from
should then move towards massive forms, into which he included cups. other organisms (Bell, 2007a; Gerovasileiou and Voultsiadou, 2016;
Should food become limited, the community would then or alterna Gerovasileiou et al., 2017).
tively tend towards erect forms. While the present proposal is well + Imagery can be more versatile than specimen collections, in that
supported by published field observations (Suppl. 2), further confir imagery and derived data are retained and can be revisited at
mation and more quantitative cause-response evaluations should be different times and used for different purposes and formats than
pursued using experimental settings. originally intended; by standardization and character annotation,
The concept of scoring sponges by their functional morphologies was resulting datasets can be reformatted and amended at any time
originally devised to enable quantitative assessment of sponge com without data loss or confusion of scored groups (Althaus et al., 2015).
munities when physical sampling is impossible. It is based on a number + Imagery represents a means of non-destructive sampling for organ
of different impulses and principles, which have advantages and dis isms of which we know little with respect to survival, regeneration
advantages, more strongly leaning towards advantages: potential and their conservation status at global scale or at the
community level (Bell et al., 2015; Schönberg, 2016b).
+ Imagery allows access to habitats where hazardous local conditions + By employing a standardised approach, growing knowledge col
prevent safe diving and thus preclude direct observations (water lecting from the scheme’s use will be comparable across different
depth, hydrodynamic conditions, wildlife, visibility; Althaus et al., studies and will increasingly improve our approaches to benthic
2015). surveys comparing sponge communities across spatial and temporal
+ In situ imagery can greatly enhance and augment already available scales, and will enable before-after-impact assessment (in contrast to
ecological and taxonomic information beyond traditional out-of- data from references in Suppl. 1).
context bench top observations (e.g., Fig. 6), even if it will never + Characterising sponge communities by dominant morphologies fa
replace measured data, taxonomic analysis and voucher collections cilitates recognition and matching of functionally similar
(e.g., Garrouste, 2017; Newcomer et al., 2019).
22
assemblages between different situations and validates the method

(Bell et al., 2006).
+ With the proposed classification scheme, imagery can be explored in
a functional context even without physical samples, at times creating
more meaningful data beyond a mere specimen count and allowing
interpretation of environmental conditions (de Laubenfels, 1936;
Schönberg and Fromont, 2013, 2019). In comparison to taxonomy-
only biodiversity assessments, scoring biological traits or ecological
functions can occasionally generate stronger information to distin
guish benthic assemblages, the habitat, or a level of disturbance at a
finer scale (Bremner et al., 2003; Bell et al., 2017). Multimetric ap
proaches in benthic surveys are thought to provide better insights
into ecosystem function and cause-response relationships where
community changes can be detected (Saito et al., 2015; here:
organismic diversity and function versus ambient conditions).
+ A deeper understanding of morphology-related traits is vitally
important in palaeoenvironmental reconstruction using fossilised
sponges (Trammer, 1979; Leinfelder et al., 1996; Krautter, 1998;
Giribet, 2015). Present, imagery-derived knowledge will support
respective efforts.
– Sponge species cannot usually be identified from imagery, and oc
casionally resulting taxonomic information will remain superficial
without physical samples.
– While imagery can be a means for data collection where physical
sampling is impossible, vouchers and reference collections are still
absolutely necessary (e.g., Suarez and Tsutsui, 2004). Classification
and data extraction from images are heatedly being discussed and
thought to lower the scientific diligence and data quality, as well
as removing lasting opportunities arising from reference collections
(e.g., Ceríaco et al., 2016; Grandcolas, 2017; Orrico, 2017; Thorpe,
2017; Newcomer et al., 2019).
– Lack of physical samples can also limit deeper insights into the
sponges’ biology in general (Homberger, 1988). Where samples can be
taken, this approach should be preferred for traditional biodiversity
assessments and to acquire additional biological data, e.g. whether
sponges are photosymbiotic or when they are reproductive. Therefore,
using the scheme we generate knowledge with respect to community
status and shifts, but we may not always understand the reasons for the
observations or physiological consequences down the line.
– Underwater imagery can only work with organisms that can still be
adequately focused during the image assessment to recognise the
phylum and the morphology. Respective datasets will thus be biased
towards larger, conspicuous individuals. Communities that mainly
consist of cryptic or small individuals such as on Carnarvon Shelf,
NW Australia (Bell et al., 2006; Schönberg and Fromont, 2012)
cannot be comprehensively surveyed in this way. Smaller, less
obvious species are generally more easily overlooked (Bell, 2007a).
Fig. 14. Imagery from towed equipment with downward capture generates a
– Image quality and angle can be an obstacle for reliable scoring. In
haphazard selection of objects that are often only partially in the frame. These
objects then appear reduced in bulk or shape due to the angle of view. The particular, images taken in turbid waters may not allow enough
shadow and other details can at times be used to access more information or to resolution, even after image enhancement (Fig. 13A-D). The vertical
better interpret the images (images were here rotated 180◦ for a more intuitive angle that is often used in towed image capture, and sponges being
angle – the light source of the towing gear usually projects the shadows for only partially captured per frame can also cause problems. However,
wards). A – From above this sponge looks like a creeping sponge, but the at times such obstacles can be overcome by local knowledge, by
shadow shows that it is erect and palmate (cf. Axos sp.). B – There large shadow assessing the sponge’s shadow (Fig. 14A-D) or by looking for char
confirms the form of the partial palmate sponge. C – Erect-laminar sponges or acteristic, group-specific details (Fig. 14E).
fans usually appear as slim bands in the images, but the shadow reveals that it – Classification and scoring accuracy from images may be lower than
has a large vertical area (Ianthella sp.). D – The large shadow suggests this is a
in a traditional taxonomy analysis (Lawler and Osborn, 2008 reached
stalked sponge, not just a low-relief cup (cf. Aplysinopsis sp. or cf. Echinodictyum
77% overall accuracy), and bias may be introduced by accuracy
clathrioides). E – At first glance this individual looks like a three-dimensionally
branching sponge, but after image enhancement and when zooming in, oscular
levels varying from morphology to morphology (Lawler and Osborn,
fields can be seen where the branches meet (arrows), revealing that this is an 2008: 56-80%). This is the reason why a standardised approach and
endopsammic sponge with branching fistules (Oceanapia sp.). well-illustrated instructions are vital.
23
Since the publication of earlier versions (Schönberg and Fromont, with widely different motives and purposes.
2013, 2014, 2019; Althaus et al., 2015), this sponge classification scheme
based on functional morphology has been applied during a number of Declaration of Competing Interest
benthic surveys in Australia (e.g., Schönberg and Fromont, 2012; Fromont
et al., 2013; Carroll et al., 2014; Przeslawski et al., 2014; Bewley et al., The author declares that she has no known competing financial in
2015; James et al., 2017). However, as the use has not previously been terest or personal relationship that could have appeared to influence the
explained in detail, some studies led to inconsistent or erroneous appli work reported in this paper.
cation. For example, an unpublished trial version in which the groups
were not yet settled was prematurely used and published (e.g., Prze Acknowledgements
slawski et al., 2013). Further, in their photo catalogue Abdul Wahab et al.
(2017) mostly identified erect-palmate (2D) forms as erect-branching (i.e., I thank all colleagues who have contributed to the development of the
as 3D), and some barrels or fistular sponges were listed as simple-massive, classification scheme and helped refining it by discussing their own ideas of
which would each reflect different responses to environmental conditions sponge morphologies and functions with me and sharing their field ob
and might have led to the inaccurate interpretation of environmental servations and practices, especially Franziska Althaus (CSIRO, Hobart,
conditions or would have been inappropriate for comparisons. However, Australia), Jane Fromont (Western Australian Museum, Perth, Australia),
this was not the aim for the photo catalogue, and the inaccurate appli Dorte Janussen (Senckenberg Institute, Frankfurt), John Hooper (Queens
cation of the present classification scheme is of little consequence in this land Museum, Brisbane, Australia) and Janie Wulff (Florida State Univer
particular case. In contrast, George et al. (2018) specifically employed this sity, Tallahassee, USA). During the sponge classification workshop held at
scheme to test the usefulness of sponge functional morphologies as envi the University of Western Australia after the 2013 World Sponge Confer
ronmental proxies, but the authors did not follow the proposed termi ence, the workshop participants tested an early version of the scheme and
nology and grouping, and the functional properties were incorrectly provided helpful feedback. Karen Gowlett-Holmes allocated CAAB
applied (see their Table 1 versus the present Tables 1–3). They erroneously numbers (CSIRO, Hobart, Australia). Muhammad Abdul Wahab (Austra
identified sponges with small attachment area as resistant to turbulence lian Institute of Marine Science, Darwin, Australia – AIMS) saved me much
(stalked and tabular forms). They stated that currents would select for time by picking out photographs with invertebrates from a towed-camera
encrusting, as well as for foliaceous (erect-laminar, 2D) morphologies, but series of images that mostly only showed mud and by looking up specimen
the latter form was lumped with erect-branching forms (3D). While parts information from the WAMSI project (Western Australian Marine Science
of the reasoning are correct, predominance of either of the three forms Institution). A large part of the SCUBA photographs, towed imagery was
would reflect different flow regimes: turbulent flow selects for encrusting, collected during surveys that were funded by WAMSI as part of the WAMSI
laminar flow for two-dimensionally erect sponges such as fans and Dredging Science Node Theme 6.3 (https://www.wamsi.org.au/dredging-
palmate forms, while reduced flow often results in the occurrence of three- science-node), and made possible through investment from Chevron
dimensionally branching sponges. George et al. (2018) implied that Australia, Woodside Energy Limited, BHP Billiton as environmental offsets
sponges respond to turbidity by expanding their horizontal area to pref and by co-investment from the WAMSI Joint Venture partners. Further
erably form massive and cup-like morphologies. However, such sponges images became available through the “Surrogates for Biodiversity” project
are more vulnerable to sediment deposition, and turbidity and sedimen of the Commonwealth Environmental Research Facilities (CERF) Marine
tation would likely rather select for erect morphologies. Moreover, the Biodiversity Hub in partnership between Geoscience Australia and the
locations for their imagery and the locations for the environmental data Australian Institute of Marine Science (https://www.nespmarine.edu.au/
measurements did not match, thus making the whole effort futile. In project/improvement-existing-and-development-new-surrogacy-relation
consequence, the authors did not find good correlations between their ships-between-physical-variables) and various AIMS research projects led
observations of the growth forms of sponge and environmental conditions by Christine Schönberg. Many people assisted during fieldwork, and the
and arrived at erroneous conclusions, e.g. that flow has no impact on following collected underwater imagery: Kim Brooks (AIMS, Perth,
sponge morphologies and that they are all roughly equally tolerant to Australia), Evy Büttner (University of Stuttgart, Germany), Flora Siebler
adverse conditions such as heat stress and storm damage. Another (University of Stuttgart, Germany), Peter Speare (AIMS, Townsville,
disadvantage inherent to previous approaches is that as a rule the choice Australia) and Janett Voigt (Christian-Albrechts University, Kiel, Ger
of used morphologies included only sponge forms that were commonly many). Various people and agencies made their images available as crea
present but did not consider what was absent and why (Suppl. 1). Where a tive commons or gave me permission to use them: Emily Crum (NOAA,
set of morphologies is not considered from start, it may become over Silver Spring, USA), Thanos Dailianis (Hellenic Centre of Marine Research,
looked. Final datasets can only provide a good understanding of the as Heraklion, Greece), Pradip Patade (Marine Life of Mumbai, India), Roberto
semblages’ functions if the investigators not only list dominant Pronzato (University of Genova, Italy), John Turnbull (Marine Explorer,
morphologies, but also consider which forms are missing, and why. Sydney, Australia), Paul Whitington (University of Melbourne, Australia)
and Samantha Wishnak (Ocean Exploration Trust, Old Lyme, USA). Steve
4. Conclusions Gill (Quekett Microscopical Club, London, Great Britain), Max Wisshak
(Senckenberg Institute, Wilhelmshaven, Germany) and Belinda Alvarez
The present publication maintains that sponges can and will respond (Biological Museum at Lund University, Sweden) are acknowledged for
to certain environmental conditions with phenotypic changes (branch providing some literature that was difficult to obtain. Oliver Gómez
patterns, oscular diameters), or selective pressures will establish a domi (Western Australian Museum, Perth, Australia) looked up collection in
nance of certain sponge growth forms represented by different species. formation. After my computer died and I could not seem to get the help I
The most influential factors in this context appear to be flow and sediment needed in time, Charles Taylor (Macs-4-U, Midland, Australia) fixed it
conditions. Both factors impact directly on the most important function in overnight. Furthermore, pre- and post-submission comments by Franziska
sponges: the way they pump water through their bodies and the physio Althaus (CSIRO, Hobart, Australia), Muhammad Abdul Wahab (AIMS,
logical processes that are supported by this. Future studies may fine-tune Darwin, Australia), Marie-Lise Schläppy (University of Western Australia
the proposed categories and identify whether there are further environ and Australian Institute of Marine Science, Perth, Australia) and Janie
mental conditions that have a direct effect on sponge morphologies and Wulff (Florida State University, Tallahassee, USA) improved the publica
how they contribute to the community structure in some yet unknown tion, and they are gratefully acknowledged, as well as efforts by peer
way. For the time being, the proposed classification scheme provides a reviewers.
valuable tool that can be used across sponge taxa, oceans and bathymetry,
enabling standardised data acquisition comparable between approaches
24
Appendix A. Supplementary data Becerro, M.A., Uriz, M.J., Turon, X., 1994. Trends in space occupation by the encrusting
sponge Crambe crambe: variation in shape as a function of size and environment.
Mar. Biol. 121, 301–307. https://doi.org/10.1007/BF00346738.
Supplementary data to this article can be found online at https://doi. Bell, J.J., 2004. Evidence for morphology-induced sediment settlement prevention on the
org/10.1016/j.ecolind.2021.107806. tubular sponge Haliclona urceolus. Mar. Biol. 146, 29–38. https://doi.org/10.1007/
s00227-004-1429-0.
Bell, J.J., 2007a. The use of volunteers for conducting sponge biodiversity assessments
References and monitoring using a morphological approach on Indo-Pacific coral reefs. Aquat.
Conserv. 17, 133–145. https://doi.org/10.1002/aqc.789.
Abdo, D.A., McDonald, J.I., Harvey, E.S., Fromont, J., Kendrick, G.A., 2008. Neighbour Bell, J.J., 2007b. Contrasting patterns of species and functional composition of coral reef
and environmental influences on the growth patterns of two temperate haliclonid sponge assemblages. Mar. Ecol. Prog. Ser. 339, 73–81. https://doi.org/10.3354/
sponges. Mar. Freshw. Res. 59, 304–312. https://doi.org/10.1071/MF07165. meps339073.
Abdo, D.A., Bellchambers, L.M., Evans, S.N., 2012. Turning up the heat: increasing Bell, J.J., Barnes, D.K., 2000a. The influences of bathymetry and flow regime upon the
temperature and coral bleaching at the high latitude coral reefs of the Houtman morphology of sublittoral sponge communities. J. Mar. Biol. Assoc. UK 80, 707–718.
Abrolhos Islands. PLoS One 7, e43878. https://doi.org/10.1371/journal. https://doi.org/10.1017/S0025315400002538.
pone.0043878. Bell, J.J., Barnes, D.K.A., 2000b. The distribution and prevalence of sponges in relation
Abdul Wahab, M.A., Gomez, O., Bryce, M., Fromont, J., 2017. Photo catalogue of marine to environmental gradients within a temperate sea lough: vertical cliff surfaces.
benthic diversity off Onslow (Pilbara Region of Western Australia). Report of project Divers. Distrib. 6, 283–303. https://doi.org/10.1046/j.1472-4642.2000.00091.x.
6.3.1 of the Dredging Science Node of the Western Australian Marine. Science Bell, J.J., Barnes, D.K.A., 2000c. The distribution and prevalence of sponges in relation to
Institution, Perth, Western Australia, p. 165 (accessed 31 March 2020). environmental gradients within a temperate sea lough: inclined cliff surfaces. Divers.
Abdul Wahab, M.A., Radford, B., Cappo, M., Colquhoun, J., Stowar, M., Depczynski, M., Distrib. 6, 305–323. https://doi.org/10.1046/j.1472-4642.2000.00092.x.
Miller, K., Heyward, A., 2018. Biodiversity and spatial patterns of benthic habitat Bell, J.J., Barnes, D.K.A., 2001a. Density, distribution and decline of two species of
and associated demersal fish communities at two tropical submerged reef unattached demosponge. Sarsia 87, 110–118. https://doi.org/10.1080/
ecosystems. Coral Reefs 37, 327–343. https://doi.org/10.1007/s00338-017-1655-9. 003648202320205184.
Abraham, E.R., 2001. The fractal branching of an arborescent sponge. Mar. Biol. 138, Bell, J.J., Barnes, D.K.A., 2001b. Sponge morphological diversity: a qualitative predictor
503–510. https://doi.org/10.1007/s002270000479. of species diversity? Aquat. Conserv. 11, 109–121. https://doi.org/10.1002/
Aerts, L.A.M., 2000. Dynamics behind standoff interactions in three reef sponge species aqc.436.
and the soral Montastraea cavernosa. PSZN Mar. Ecol. 21, 191–204. https://doi.org/ Bell, J.J., Barnes, D.K., 2002. Modelling sponge species diversity using a morphological
10.1046/j.1439-0485.2000.00685.x. predictor: a tropical test of a temperate model. J. Nat. Conserv. 10, 41–50. https://
Aerts, L.A.M., van Soest, R.W.M., 1997. Quantification of sponge/coral interactions in a doi.org/10.1078/1617-1381-00005.
physically stressed reef community, NE Colombia. Mar. Ecol. Prog. Ser. 148, Bell, J.J., Barnes, D.K.A., Shaw, C., 2002a. Branching dynamics of two species of
125–134. https://doi.org/10.3354/meps148125. arborescent demosponge: the effect of flow regime and bathymetry. J. Mar. Biol.
Althaus, F., Hill, N., Edwards, L., Ferrari, R., 2014. CATAMI Classification Scheme for Assoc. UK 82, 279–294. https://doi.org/10.1017/S0025315402005465.
scoring marine biota and substrata in underwater imagery. A pictorial guide to the Bell, J.J., Barnes, D.K.A., Turner, J., 2002b. The importance of micro and macro
Collaborative and Automated Tools for Analysis of Marine Imagery (CATAMI) morphological variation in the adaptation of a sublittoral demosponge to current
classification scheme. Version 1.4 – December 2014. Marine Biodiversity Hub. extremes. Mar. Biol. 140, 75–81. https://doi.org/10.1007/s002270100665.
National Environmental Science Programme, Hobart. http://catami.github.io/cat Bell, J.J., Barnes, D.K., 2003. The importance of competitor identity, morphology and
ami-docs/CATAMI%20class_PDFGuide_V4_20141218.pdf (accessed 28 February ranking methodology to outcomes in interference competition between sponges.
2020). Mar. Biol. 143, 415–426. https://doi.org/10.1007/s00227-003-1081-0.
Althaus, F., Hill, N., Ferrari, R., Edwards, L., Przeslawski, R., Schönberg, C.H.L., Stuart- Bell, J.J., Bennett, H.M., Rovellini, A., Webster, N.S., 2018. Sponges to be winners under
Smith, R., Barrett, N., Edgar, G., Colquhoun, J., Tran, M., Jordan, A., Rees, T., near-future climate scenarios. Bioscience 68, 955–968. https://doi.org/10.1093/
Gowlett-Holmes, K., 2015. A standardised vocabulary for identifying benthic biota biosci/biy142.
and substrata from underwater imagery: the CATAMI classification scheme. PLoS Bell, J.J., Biggerstaff, A., Bates, T., Bennett, H., Marlow, J., McGrath, E., Shaffer, M.,
ONE 10, e 0141039. https://doi.org/10.1371/journal.pone.0141039. 2017. Sponge monitoring: moving beyond diversity and abundance measures. Ecol.
Alvarez, B., Browne, M.F., Horner, S., 2002. Sponge biodiversity in Darwin Harbour, Ind. 78, 470–488. https://doi.org/10.1016/j.ecolind.2017.03.001.
Northern Territory, Australia. Boll. Mus. Ist. Biol. Univ. Genova 66–67, 10. Bell, J.J., Burton, M., Bullimore, B., Newman, P.B., Lock, K., 2006. Morphological
Alvarez-Filip, L., Dulvy, N.K., Côté, I.M., Watkinson, A.R., Gill, J.A., 2011. Coral identity monitoring of subtidal sponge assemblages. Mar. Ecol. Prog. Ser. 311, 79–91.
underpins architectural complexity on Caribbean reefs. Ecol. Appl. 21, 2223–2231. https://doi.org/10.3354/meps311079.
https://www.jstor.org/stable/41416650. Bell, J.J., McGrath, E., Biggerstaff, A., Bates, T., Cárdenas, C.A., Bennett, H., 2015. Global
Álvarez-Noriega, M., Baird, A.H., Dornelas, M., Madin, J.S., Cumbo, V.R., Connolly, S.R., conservation status of sponges. Conserv. Biol. 29, 42–53. https://doi.org/10.1111/
2016. Fecundity and the demographic strategies of coral morphologies. Ecology 97, cobi.12447.
3485–3493. https://doi.org/10.1002/ecy.1588. Bellwood, D.R., Streit, R.P., Brandl, S.J., Tebbett, S.B., 2019. The meaning of the term
Ashok, A.M., Schönberg, C.H.L., Raj, K.D., Bhoopathi, M., Bharath, M.S., Patterson, E.J., ‘function’ in ecology: A coral reef perspective. Funct. Ecol. 3, 948–961. https://doi.
2018. A sponge of the Cliona viridis complex invades and excavates corals of the Gulf org/10.1111/1365-2435.13265.
of Mannar, south-eastern India. Mar. Freshw. Res. 69, 874–882. https://doi.org/ Bergquist, P.R., 1978. Sponges. University of California Press, Berkeley, Los Angeles,
10.1071/MF17247. p. 267. https://doi.org/10.1038/npg.els.0001582.
Ayling, A.L., 1983. Growth and regeneration rates in thinly encrusting Demospongiae Berman, J., Burton, M., Gibbs, R., Lock, K., Newman, P., Jones, J., Bell, J., 2013. Testing
from temperate waters. Biol. Bull. 165, 343–352. the suitability of a morphological monitoring approach for identifying temporal
Balata, D., Piazzi, L., Rindi, F., 2011. Testing a new classification of morphological variability in a temperate sponge assemblage. J. Nat. Conserv. 21, 173–182. https://
functional groups of marine macroalgae for the detection of responses to stress. Mar. doi.org/10.1016/j.jnc.2012.12.003.
Biol. 158, 2459–2469. https://doi.org/10.1007/s00227-011-1747-y. Bewley, M., Friedman, A., Ferrari, R., Hill, N., Hovey, R., Barrett, N., Marzinelli, E.M.,
Bannister, R.J., Brinkman, R., Wolff, C., Battershill, C., de Nys, R., 2007. The distribution Pizarro, O., Figueira, W., Meyer, L., Babcock, R., Bellchambers, L., Byrne, M.,
and abundance of dictyoceratid sponges in relation to hydrodynamic features: Williams, S.B., 2015. Australian sea-floor survey data, with images and expert
identifying candidates and environmental conditions for sponge aquaculture. Mar. annotations. Sci. Data 3, 150057. https://doi.org/10.1038/sdata.2015.57.
Freshw. Res. 58, 624–633. https://doi.org/10.1071/MF07011. Bibiloni, M.A., Uriz, M.J., Gili, J.M., 1989. Sponge communities in three submarine caves
Barnes, D.K.A., 1999. High diversity of tropical intertidal zone sponges in temperature, of the Balearic Islands (Western Mediterranean): adaptations and faunistic
salinity and current extremes. Afr. J. Ecol. 37, 424–434. https://doi.org/10.1046/ composition. Mar. Ecol. 10, 317–334. https://doi.org/10.1111/j.1439-0485.1989.
j.1365-2028.1999.00197.x. tb00076.x.
Barnes, D.K.A., Bell, J.J., 2002. Coastal sponge communities of the West Indian Ocean: Bidder, G.P. 1923. The relation of the form of a sponge to its currents. Q. J. Microsc. Sci.
morphological richness and diversity. Afr. J. Ecol. 40, 350–359. https://doi.org/ 67, 293–323. Accessed April 15, 2020. https://jcs.biologists.org/content/joces/s2-
10.1046/j.1365-2028.2002.00388.x. 67/266/293.full.pdf.
Barnes, P.B., Davis, A.R., Roberts, D.E., 2006. Sampling patchily distributed taxa: a case Biggs, B.C., 2013. Harnessing natural recovery processes to improve restoration
study using cost-benefit analyses for sponges and ascidians in coastal lakes of New outcomes: an experimental assessment of sponge-mediated coral reef restoration.
South Wales, Australia. Mar. Ecol Prog. Ser. 31, 55–64. https://doi.org/10.3354/ PLoS ONE 8, e64945. https://doi.org/10.1371/journal.pone.0064945.
meps319055. Blakeway, D., Byers, M., Stoddart, J., Rossendell, J., 2013. Coral colonisation of an
Barnes, P.B., Roberts, D.E., Davis, A.R., 2013. Biodiversity in saline coastal lagoons: artificial reef in a turbid nearshore environment, Dampier Harbour, Western
patterns of distribution and human impacts on sponge and ascidian assemblages. Australia. PLoS ONE 8, e75281. https://doi.org/10.1371/journal.pone.0075281.
Divers. Distrib. 19, 1394–1406. https://doi.org/10.1111/ddi.12108. Bonsdorff, E., Pearson, T.H., 1999. Variation in the sublittoral macrozoobenthos of the
Barrett, N., Seiler, J., Anderson, T., Williams, S., Nichol, S., Hill, S.N., 2010. Autonomous Baltic Sea along environmental gradients: a functional-group approach. Aust. J. Ecol.
Underwater Vehicle (AUV) for mapping marine biodiversity in coastal and shelf 24, 312–326. https://doi.org/10.1046/j.1442-9993.1999.00986.x.
waters: implications for marine management. Proc. Oceans’ 10 IEEE Conf., Sydney, Boury-Esnault, N., Rützler, K., 1997. Thesaurus of sponge morphology. Smithsonian
24–27 May 2010, 1–6. 10.1109/OCEANSSYD.2010.5603860. Contrib. Zool. 596, 1–55.
Barthel, D., Gutt, J., 1992. Sponge associations in the eastern Weddell Sea. Antarctic Sci. Bremner, J., Rogers, S.I., Frid, C.L.J., 2003. Assessing functional diversity in marine
4, 137–150. https://doi.org/10.1017/S0954102092000221. benthic ecosystems: a comparison of approaches. Mar. Ecol. Prog. Ser. 254, 11–25.
https://doi.org/10.3354/meps254011.
25
Brocx, M., Semeniuk, V., 2017. Impacts of ports along the Pilbara Coast, Western Edgar, G.J., Stuart-Smith, R.D., 2009. Ecological effects of marine protected areas on
Australia – a coastline of global geoheritage significance that services a mineral-rich rocky reef communities – a continental-scale analysis. Mar. Ecol. Prog. Ser. 388,
hinterland. Ann. Geophys. 60, 1–12. https://doi.org/10.4401/ag-7495. 51–62. https://doi.org/10.3354/meps08149.
Caldicott, D.G., Croser, D., Manolis, C., Webb, G., Britton, A., 2005. Crocodile attack in Emslie, M.J., Cheal, A.J., Sweatman, H., Delean, S., 2008. Recovery from disturbance of
Australia: an analysis of its incidence and review of the pathology and management coral and reef fish communities on the Great Barrier Reef. Australia. Mar. Ecol. Prog.
of crocodilian attacks in general. Wild. Environ. Med. 16, 143–159. https://doi.org/ Ser. 371, 177–190. https://doi.org/10.3354/meps07657.
10.1580/1080-6032(2005)16[143:CAIAAA]2.0.CO;2. Fromont, J., 2004. Porifera (sponges) of the Dampier Archipelago, Western Australia:
Cambridge, M.L., McComb, A.J., 1984. The loss of seagrasses in Cockburn Sound, habitats and distributions. Rec. Western Australian Mus. 66, 69–100. https://doi.
Western Australia. I. The time course and magnitude of seagrass decline in relation org/10.18195/issn.0313-122x.66.2004.069-100.
to industrial development. Aquat. Bot. 20, 229–243. https://doi.org/10.1016/0304- Fromont, J., Abdul Wahab, M.A., Gomez, O., Ekins, M., Grol, M., Hooper, J.N.A., 2016.
3770(84)90089-5. Patterns of sponge biodiversity in the Pilbara, northwestern Australia. Diversity 8,
Carballo, J.L., Naranjo, S.A., García-Gómez, J.C., 1996. Use of marine sponges as stress 21. https://doi.org/10.3390/d8040021.
indicators in marine ecosystems at Algeciras Bay (southern Iberian Peninsula). Mar. Fromont, J., Althaus, F., McEnnulty, F.R., Williams, A., Salotti, M., Gomez, O., Gowlett-
Ecol. Prog. Ser. 135, 109–122. https://doi.org/10.3354/meps135109. Holmes, K., 2011. Living on the edge: the sponge fauna of Australia’s southwestern
Carballo, J.L., Vega, C., Cruz-Barraza, J.A., Yanez, B., Nava, H., Avila, E., Wilson, M., and northwestern deep continental margin. Hydrobiologia 687, 127–142. https://
2008. Short-and long-term patterns of sponge diversity on a rocky tropical coast: doi.org/10.1007/978-94-007-4688-6_12.
evidence of large-scale structuring factors. Mar. Ecol. 29, 216–236. https://doi.org/ Fromont, J., Vanderklift, M.A., Kendrick, G.A., 2006. Marine sponges of the Dampier
10.1111/j.1439-0485.2008.00228.x. Archipelago, Western Australia: patterns of species distributions, abundance and
Carroll, A., Tran, M., Przeslawski, R., 2014. Use of underwater videography and still diversity. In: Hawksworth, D.L., Bull, A.T. (Eds.), Marine, Freshwater, and Wetlands
imagery for sponge biodiversity habitat mapping and modelling. F1000 Res. 5, Biodiversity Conservation. Topics in Biodiversity and Conservation 4. Springer,
1095360 (accessed 11 March 2020). https://f1000research.com/slides/1095360. Dordrecht, pp. 363–382. https://doi.org/10.1007/978-1-4020-5734-2_24.
Carter, H.J., 1882. Some sponges from the West Indies and Acapulco in the Liverpool Fromont, J., Schönberg, C., Speare, P., Gomez, O., Büttner, E., Siebler, F., 2013. Sponges
Free Museum described, with general and classificatory remarks. Ann. Mag. Nat. in a dust cloud: dredging related pressures in NW Australia. F1000 Res. 1094711
Hist. 9, 266–301, 346–368, pls. XI–XII. https://doi.org/10.1080/00222938 (accessed 28 March 2020). https://f1000research.com/slides/1094711.
209459052. Fromont, J., Sampey, A. 2014. Kimberley marine biota. Historical data: sponges
Ceríaco, L.M., Gutiérrez, E.E., Dubois, A., Carr, M. 2016. Photography-based taxonomy is (Porifera). Rec. Western Australian Mus., Suppl. 84, 69–100. https://doi.org/10.181
inadequate, unnecessary, and potentially harmful for biological sciences. Zootaxa 95/issn.0313-122x.84.2014.069-100.
4196, 435–s445. https://doi.org/10.11646/zootaxa.4196.3.9. Fromont, J., Vanderklift, M.A., 2009. Porifera (sponges) of Mermaid, Scott and
Cerrano, C., Bavestrello, G., Boyer, M., Calcinai, B., Lalamentik, L.T.X., Pansini, M. 2002. Seringapatam Reefs, north Western Australia. Rec. Western Australian Mus. Suppl.
Psammobiontic sponges from the Bunaken Marine Park (North Sulawesi, Indonesia): 77, 89–103. 10.18195/issn.0313-122x.77.2009.089-103.
interactions with sediments. Proc. 9th Int. Coral Reef Symp., Bali 23–27 October Fry, W.G., 1979. Taxonomy, the individual and the sponge. In: Larwood, G., Rosen, B.R.
2000, vol. 1, 279–282. (Eds.), Biology and Systematics of Colonial Organisms. The Systematics Association
Chabanet, P., Adjeroud, M., Andréfouët, S., Bozec, Y.-M., Ferraris, J., Garcìa-Charton, J.- Special, Volume 11. Academic Press, London, New York, San Francisco, pp. 49–80.
A., Schrimm, M., 2005. Human-induced physical disturbances and their indicators Fry, W.G., Fry, P.D., 1979. Aspects of the functional anatomy and ecological physiology
on coral reef habitats: a multi-scale approach. Aquat. Living Resour. 18, 215–230. of Disyringa and some other infaunal tetractinomorph sponges, In: Lévi, C., Boury-
https://doi.org/10.1051/alr:2005028. Esnault, N. (Eds.), Biologie des Spongiaires, Coll. Int. Centre Nat. Rech. Sci. 291.
Chombard, C., Boury-Esnault, N., 1999. Good congruence between morphology and Centre National de la Recherche Scientifique, Paris, pp. 335-341.
molecular phylogeny of Hadromerida, or how to bother sponge taxonomists. Mem. Garrabou, J., Gómez-Gras, D., Ledoux, J.B., Linares, C., Bensoussan, N., López-
Queensland Mus. 44, 100. Sendino, P., Bazairi, H., Espinosa, F., Ramdani, M., Grimes, S., Benabdi, M.,
Cleary, D.F.R., de Voogd, N.J., 2007. Environmental associations of sponges in the Souissi, J.B., Soufi, E., Khamassi, F., Ghanem, R., Ocaña, O., Ramos-Esplà, A.,
Spermonde Archipelago. Indonesia. J. Mar. Biol. Assoc. UK 87, 1669–1676. https:// Izquierdo, A., Anton, I., Rubio-Portillo, E., Barbera, C., Cebrian, E., Marbà, N.,
doi.org/10.1017/S0025315407052770. Hendriks, I.E., Duarte, C.M., Deudero, S., Díaz, D., Vázquez-Luis, M., Alvarez, E.,
Collins, J.H., 2008. Marine tourism in the Kimberley region of Western Australia. Geog. Hereu, B., Kersting, D.K., Gori, A., Viladrich, N., Sartoretto, S., Pairaud, I.,
Res. 46, 111–123. https://doi.org/10.1111/j.1745-5871.2007.00496.x. Ruitton, S., Pergent, G., Pergent-Martini, C., Rouanet, E., Teixidó, N., Gattuso, J.-P.,
Costello, M.J., Coll, M., Danovaro, R., Halpin, P., Ojaveer, H., Miloslavich, P., 2010. Fraschetti, S., Rivetti, I., Azzurro, E., Cerrano, C., Ponti, M., Turicchia, E.,
A census of marine biodiversity knowledge, resources, and future challenges. PLoS Bavestrello, G., Cattaneo-Vietti, R., Bo, M., Bertolino, M., Montefalcone, M.,
ONE 5, e12110. https://doi.org/10.1371/journal.pone.0012110. Chimienti, G., Grech, D., Rilov, G., Tuney Kizilkaya, I., Kizilkaya, Z., Topçu, N.E.,
Cummings, V.J., Beaumont, J., Mobilia, V., Bell, J.J., Tracey, D., Clark, M.R., Barr, N., Gerovasileiou, V., Sini, M., Bakran-Petricioli, T., Kipson, S., Harmelin, J.G., 2019.
2020. Responses of a common New Zealand coastal sponge to elevated suspended Collaborative database to track mass mortality events in the Mediterranean Sea.
sediments: indications of resilience. Mar. Environ. Res. 155, 104886. https://doi. Frontiers Mar. Sci. 6, 707. https://doi.org/10.3389/fmars.2019.00707.
org/10.1016/j.marenvres.2020.104886. Garrouste, R., 2017. The “wild shot”: photography for more biology in natural history
Currie, D.R., Isaacs, L.R., 2005. Impact of exploratory offshore drilling on benthic collections, not for replacing vouchers. Zootaxa 4269, 453–454. https://doi.org/10.
communities in the Minerva gas field, Port Campbell. Australia. Mar. Environ. Res. 11646/zootaxa.4269.4.2.
59, 217–233. https://doi.org/10.1016/j.marenvres.2004.05.001. Gaino, E., Pronzato, R., Corriero, G., Buffa, P., 1992. Mortality of commercial sponges:
Currie, D.R., Sorokin, S.J., 2014. Megabenthic biodiversity in two contrasting submarine incidence in two Mediterranean areas. Italian J. Zool. 59, 79–85. https://doi.org/
canyons on Australia’s southern continental margin. Mar. Environ. Res. 10, 97–110. 10.1080/11250009209386652.
https://doi.org/10.1080/17451000.2013.797586. George, A.M., Brodie, J., Daniell, J., Capper, A., Jonker, M., 2018. Can sponge
DeBiasse, M.B., Hellberg, M.E., 2015. Discordance between morphological and molecular morphologies act as environmental proxies to biophysical factors in the Great Barrier
species boundaries among Caribbean species of the reef sponge Callyspongia. Ecol. Reef, Australia? Ecol. Ind. 93, 1152–1162. https://doi.org/10.1016/j.
Evol. 5, 663–675. https://doi.org/10.1002/ece3.1381. ecolind.2018.06.016.
De Laubenfels, M.W., 1936. The ecology of the Porifera, and possibilities of deductions as Gerovasileiou, V., Dimitriadis, C., Arvanitidis, C., Voultsiadou, E., 2017. Taxonomic and
to the paleoecology of sponges from their fossils. Rep. Committee Paleoecol., 1935- functional surrogates of sessile benthic diversity in Mediterranean marine caves.
1936. App. J Ann. Rep. Div. Geol. and Geogr. Nat. Res. Council, 2 May 1936, 44–54. PLoS ONE 12, e0183707. https://doi.org/10.1371/journal.pone.0183707.
Denis, V., Ribas-Deulofeu, L., Sturaro, N., Kuo, C.Y., Chen, C.A., 2017. A functional Gerovasileiou, V., Voultsiadou, E., 2016. Sponge diversity gradients in marine caves of
approach to the structural complexity of coral assemblages based on colony the eastern Mediterranean. J. Mar. Biol. Assoc. UK 96, 407–416. https://doi.org/
morphological features. Sci. Rep. 7, 1–11. https://doi.org/10.1038/s41598-017- 10.1017/S0025315415000697.
10334-w. Gershwin, L.A. 2005. Two new species of jellyfishes (Cnidaria: Cubozoa: Carybdeida)
Denny, M.W., 1994. Extreme drag forces and the survival of wind and water-swept from tropical Western Australia, presumed to cause Irukandji Syndrome. Zootaxa
organisms. J. Exp. Biol. 194, 97–115. https://doi.org/10.1242/jeb.194.1.97. 1084, 1–30. https://doi.org/10.11646/zootaxa.1084.1.1.
Denny, M.W., Daniel, T.L., Koehl, M.A.R., 1985. Mechanical limits to size in wave-swept Gibbs, L., Warren, A., 2015. Transforming shark hazard policy: learning from ocean-users
organisms. Ecol. Monogr. 55, 69–102. https://doi.org/10.2307/1942526. and shark encounter in Western Australia. Mar. Policy 58, 116–124. https://doi.org/
Depczynski, M., Gilmour, J.P., Ridgway, T., Barnes, H., Heyward, A.J., Holmes, T.H., 10.1016/j.marpol.2015.04.014.
Moore, J.A.Y., Radford, B.T., Thomson, D.P., Tinkler, P., Wilson, S.K., 2013. Gilliam, D.S., Walker, B.K., Saelens, S.J., Fahy, D.P., Kosmynin, V.N., 2009. Recovery of
Bleaching, coral mortality and subsequent survivorship on a West Australian fringing injured giant barrel sponges, Xestospongia muta, offshore southeast Florida. Proc.
reef. Coral Reefs 32, 233–238. https://doi.org/10.1007/s00338-012-0974-0. 11th Int. Coral Reef Symp., Ft. Lauderdale, Florida, 7-11 July 2008, 1230–1234. htt
De Voogd, N.J., Cleary, D.F.R., 2007. Relating species traits to environmental variables in ps://pdfs.semanticscholar.org/4ba0/4d492fcfea5866e1b6671980b3d8ea00f07e.
Indonesian coral reef sponge assemblages. Mar. Freshw. Res. 58, 240–249. https:// pdf?_ga=2.80267607.1701335113.1586937740-37424417.1578360261 (accessed
doi.org/10.1071/MF06125. 15 April 2020).
De Voogd, N.J., Cleary, D.F.R., 2009. Variation in sponge composition among Singapore Gilmour, J.P., Cook, K.L., Ryan, N.M., Puotinen, M.L., Green, R.H., Shedrawi, G.,
reefs. Raffles Bull. Zool. Suppl. 22, 59–67. Hobbs, J.P.A., Thomson, D.P., Babcock, R.C., Buckee, J., Foster, T., Richards, Z.T.,
Divine, L.M., 2011. Effects of sediment on growth and survival of various juvenile Wilson, S.K., Wilson, P.B., Coutts, T.B., Radford, B.T., Piggott, C.H., Depczynski, M.,
morphologies of the scleractinian coral, Oculina arbuscula (Verrill). MSc thesis at the Evans, S.N., Schoepf, V., Evans, R.D., Halford, A.R., Nutt, C.D., Bancroft, K.P.,
Georgia Southern University, Statesboro, 79 pp. Heyward, A.J., Oades, D., 2019. The state of Western Australia’s coral reefs. Coral
Duran, S., Rützler, K., 2006. Ecological speciation in a Caribbean marine sponge. Mol. Reefs 38, 651–667. https://doi.org/10.1007/s00338-019-01795-8.
Phylogenet. Evol. 40, 292–297. https://doi.org/10.1016/j.ympev.2006.02.018.
26
Giribet, G., 2015. Morphology should not be forgotten in the era of genomics – a Mediterranean). ICES J. Mar. Sci. 60, 402–410. https://doi.org/10.1016/S1054-
phylogenetic perspective. Zool. Anz. 256, 96–103. https://doi.org/10.1016/j. 3139(03)00012-2.
jcz.2015.01.003. Kenchington, R., Hutchings, P., 2012. Science, biodiversity and Australian management
Gochfeld, D.J., Olson, J.B., Chaves-Fonnegra, A., Smith, T.B., Ennis, R.S., Brandt, M.E., of marine ecosystems. Ocean Coast. Manag. 69, 194–199. https://doi.org/10.1016/j.
2020. Impacts of hurricanes Irma and Maria on coral reef sponge communities in St. ocecoaman.2012.08.009.
Thomas. US Virgin Islands. Est. Coasts 43, 1–13. https://doi.org/10.1007/s12237- Kirkendale, L., Hosie, A.M., Richards, Z., 2019. Defining biodiversity gaps for North West
020-00694-4. Shelf marine invertebrates. J. Royal Soc. Western Australia 102, 1–9.
Goudie, L., Norman, M., Finn, J., 2013. Sponges. Museum Victoria Field Guides to Knowlton, N., 2000. Molecular genetic analyses of species boundaries in the sea.
Marine Life. Museum Victoria Publishing, Melbourne, p. 134. Hydrobiologia 420, 73–90. https://doi.org/10.1007/978-94-017-2184-4_8.
Grandcolas, P. 2017. Losing the connection between the observation and the specimen: a Könnecker, G., 1973. Littoral and benthic investigations on the west coast of Ireland – I.
by-product of the digital era or a trend inherited from general biology? Bionomia 12, (Section A: faunistic and ecological studies). The sponge fauna of Kilkieran Bay and
57–62. https://doi.org/10.11646/bionomina.12.1.7. adjacent areas. Proc. Royal Irish Acad. Sect. B: Biol. Geol. Chem. Sci. 73, 451–472.
Gruber, R.K., Lowe, R.J., Falter, J.L., 2017. Metabolism of a tide-dominated reef platform https://www.jstor.org/stable/20518931.
subject to extreme diel temperature and oxygen variations. Limnol. Oceanogr. 62, Krautter, M., 1998. Ecology of siliceous sponges – application to the environmental
1701–1717. https://doi.org/10.1002/lno.10527. interpretation of the Upper Jurassic sponge facies (Oxfordian) from Spain. Cuad.
Gutt, J., 2007. Antarctic macro-zoobenthic communities: a review and an ecological Geol. Ibérica 24, 223–239.
classification. Antarctic Sci. 19, 165–ß182. https://doi.org/10.1017/S0954102 Kullmann, K., 2014. The emergence of suburban terracing on coastal dunes: case studies
007000247. along the Perth Northern Corridor, Western Australia, 1930–2010. J. Urban Design
Hadi, T.A., Hadiyanto, Budiyanto, A., Wentao, N., Suharsono, 2015. The morphological 19, 593–621. https://doi.org/10.1080/13574809.2014.943704.
and species diversity of sponges on coral reef ecosystems in the Lembeh Strait, Lafratta, A., Fromont, J., Speare, P., Schönberg, C.H.L., 2017. Coral bleaching in turbid
Bitung. Mar. Res. Indonesia 40, 65–77. https://doi.org/10.14203/mri.v40i2.45. waters of north-western Australia. Mar. Freshw. Res. 68, 65–75. https://doi.org/
Hajdu, E., Vacelet, J. 2002. Family Cladorhizidae Dendy, 1922, In: Hooper, J.N.A., van 10.1071/MF15314.
Soest, R.W.M. (Eds.), Systema Porifera. A Guide to the Classification of Sponges. Vol. Last, P.R., Lyne, V.D., Williams, A., Davies, C.R., Butler, A.J., Yearsley, G.K., 2010.
1. Kluwer Academic, Plenum Publishers, New York, Boston, Dordrecht, London, A hierarchical framework for classifying seabed biodiversity with application to
Moscow, pp. 636–641. https://doi.org/10.1007/978-1-4615-0747-5_1. planning and managing Australia’s marine biological resources. Biol. Conserv. 143,
Hall, K.A., Hooper, J.N.A., 2019. SpongeMaps - an Online Community for Sponge 1675–1686. https://doi.org/10.1016/j.biocon.2010.04.008.
Taxonomy. https://www.spongemaps.org/ (accessed 4 May 2020). Lauder, G.V., 1990. Functional morphology and systematics: studying functional patterns
Hercock, M., 1999. The impacts of recreation and tourism in the remote North Kimberly in an historical context. Ann. Rev. Ecol. Syst. 21, 317–340. https://doi.org/10.1146/
region of Western Australia. Environmentalist 19, 259–275. https://doi.org/ annurev.es.21.110190.001533.
10.1023/A:1026406912992. Lawler, M.M., Osborn, J.E., 2008. Photogrammetric classification of sponge
Heyward, A., Fromont, J., Schönberg, C.H.L., Colquhoun, J., Radford, B., Gomez, O., morphometric diversity. 14th Australian Remote Sensing Photogramm. Conf., 29
2010. The sponge gardens of Ningaloo reef. Western Australia. Open Mar. Biol. J. 4, September – 3 October 2008, Darwin, 1–12. https://eprints.utas.edu.au/8385/
3–11. https://doi.org/10.2174/1874450801004010003. (accessed 27 January 2020).
Hill, M.S., 1999. Morphological and genetic examination of phenotypic variability in the Leal, C.V., de Paula, T.S., Lôbo-Hajdu, G., Schönberg, C.H.L., Esteves, E.L., 2016.
tropical sponge Anthosigmella varians. Mem. Queensland Mus. 44, 239–248. Morphological and molecular systematics of the “Cliona viridis complex” from south-
Hiscock, K., 1983. Water movement. In: Earll, R., Erwin, D.G. (Eds.), Sublittoral Ecology. eastern Brazil. J. Mar. Biol. Assoc. UK 96, 313–322. https://doi.org/10.1017/
The Ecology of the Shallow Sublittoral Benthos. Clarendon Press, Oxford, pp. 58–96. S0025315415001642.
Hoffmann, F., Rapp, H.T., Pape, T., Peters, H., Reltner, J., 2004. Sedimentary inclusions Lee, W.L., Reiswig, H.M., Austin, W.C., Lundsten, L., 2012. An extraordinary new
in the deep-wate sponge Geodia barretti (Geodiidae, Demospongiae) from the carnivorous sponge, Chondrocladia lyra, in the new subgenus Symmetrocladia
Korsfjord, western Norway. Sarsia 89, 245–252. https://doi.org/10.1080/ (Demospongiae, Cladorhizidae), from off of northern California. USA. Invertebr.
00364820410002451. Biol. 131, 259–284. https://doi.org/10.1111/ivb.12001.
Homberger, D.G., 1988. Models and tests in functional morphology: the significance of Leinfelder, R.R., Werner, W., Nose, M., Schmid, D.U., Krautter, M., Laternser, R.,
description and integration. Amer. Zool. 28, 217–229. https://doi.org/10.1093/icb/ Takacs, M., Hartmann, M., 1996. Paleoecology, growth parameters and dynamics of
28.1.217. coral, sponge and microbolite reefs from the Late Jurassic. Göttinger Arb. Geol.
Hooper, J.N.A., Bergquist, P.R., 1992. Cymbastela, a new genus of lamellate coral reef Paläont. Special 2, 227–248.
sponges. Mem. Queensland Mus. 32, 99–137. Le Nohaïc, M., Ross, C.L., Cornwall, C.E., Comeau, S., Lowe, R., McCulloch, M.T.,
Hooper, J.N.A., Ekins, M., 2004. Collation and validation of museum collection databases Schoepf, V., 2017. Marine heatwave causes unprecedented regional mass bleaching
related to the distribution of marine sponges in northern Australia. Tech. Rep. of thermally resistant corals in northwestern Australia. Sci. Rep. 7, 14999. https://
Queensland Mus. 2, 1–224. doi.org/10.1038/s41598-017-14794-y.
Hooper, J.N.A., Hall, K.A., Ekins, M., Erpenbeck, D., Wörheide, G., Jolley-Rogers, G., Lim, S.C., de Voogd, N., Siang, T.K., 2008. A Guide to Sponges of Singapore. Science
2013. Managing and sharing the escalating number of sponge “unknowns”: the Centre, Singapore, p. 173.
SpongeMaps project. Integr. Comp. Biol. 53, 473–481. https://doi.org/10.1093/icb/ López-Legentil, S., Erwin, P.M., Henkel, T.P., Loh, T.L., Pawlik, J.R., 2010. Phenotypic
ict038. plasticity in the Caribbean sponge Callyspongia vaginalis (Porifera: Haplosclerida).
Hooper, J.N.A., Kennedy, J.A., 2002. Small-scale patterns of sponge biodiversity Sci. Mar. 74, 445–453. https://doi.org/10.3989/scimar.2010.74n3445.
(Porifera) from the Sunshine Coast reefs, eastern Australia. Invertebr. Syst. 16, Maldonado, M., Young, C.M., 1996. Bathymetric patterns of sponge distribution on the
637–653. https://doi.org/10.1071/IS02015. Bahamian slope. Deep Sea Res. Part I Oceanogr. Res. Papers 43, 897–915. https://
Hooper, J., Kennedy, J.A., List-Armitage, S.E., Cook, S.D., Quinn, R., 1999. Biodiversity, doi.org/10.1016/0967-0637(96)00042-8.
species composition and distribution of marine sponges in northeast Australia. Mem. Makowski, C., Prekel, S.E., Lybolt, M.J., Baron, R.M., 2009. The benthic ecological
Queensland Mus. 44, 263–274. assessment for marginal reefs (BEAMR) method. J. Coast. Res. 25, 515–522. https://
Hooper, J.N.A., Kennedy, J.A., Quinn, R.J., 2002. Biodiversity “hotspots”, patterns of doi.org/10.2112/08-1123.1.
richness and endemism, and taxonomic affinities of tropical Australian sponges Marlow, J., Bell, J.J., Schaffer, M., Haris, A., Schönberg, C.H.L., in press. Bioeroding
(Porifera). Biodiv. Conserv. 11, 851–885. https://doi.org/10.1023/A: sponge species from the Wakatobi region of southeast Sulawesi, Indonesia. Zootaxa.
1015370312077. Mawson, P., 2004. Crocodile management in Western Australia. In: Crocodiles. Proc.
Jackson, J.B.C., 1979. Morphological strategies of sessile animals. In: Larwood, G., 17th Working Meeting Crocodile Specialist Group Species Survival Comm. Int. Union
Rosen, B.R. (Eds.), Biology and Systematics of Colonial Organisms. The Systematics Conserv. Nature – The World Conservation Union, Gland, Switzerland, and
Association Special, Volume 11. Academic Press, London, New York, San Francisco, Cambridge, UK, Darwin, Australia. IUCN-SSC Crocodile Specialist Group, Karama,
pp. 499–555. Australia, 28–37.
James, L.C., Marzloff, M.P., Barrett, N., Friedman, A., Johnson, C.R., 2017. Changes in May, R.F., 1992. Marine conservation reserves, petroleum exploration and development,
deep reef benthic community composition across a latitudinal and environmental and oil spills in coastal waters of Western Australia. Mar. Pollut. Bull. 25, 147–154.
gradient in temperate Eastern Australia. Mar. Ecol. Prog. Ser. 565, 35–52. https:// https://doi.org/10.1016/0025-326X(92)90218-U.
doi.org/10.3354/meps11989. McAuley, R., Bruce, B., Keay, I., Mountford, S., Tania, P., 2016. Evaluation of passive
Jones, W.C., 1994. Process-formation by aquarium-kept sponges and its relevance to acoustic telemetry approaches for monitoring and mitigating shark hazards off the
sponge ecology and taxonomy. In: van Soest, R.W.M., van Kempen, T.M.G., coast of Western Australia. Fisheries Research Report 273, 2016 North Beach,
Braekman, J.C. (Eds.), Sponges in Time and Space. Biology. Chemistry, Department of Fisheries, Government of Western Australia, 84 pp.
Paleontology. Balkema, Rotterdam, Brookfield, pp. 241–249. McDonald, J.I., Hooper, J.N.A., McGuinness, K.A., 2002. Environmentally influenced
Kaandorp, J.A., 1991. Modelling growth forms of the sponge Haliclona oculata (Porifera, variability in the morphology of Cinachyrella australiensis (Carter, 1886) (Porifera:
Demospongiae) using fractal techniques. Mar. Biol. 110, 203–215. https://doi.org/ Spirophorida: Tetillidae). Mar. Freshw. Res. 53, 79–84. https://doi.org/10.1071/
10.1007/BF01313706. MF00153.
Kaandorp, J.A., de Kluijver, M.J., 1992. Verification of fractal growth models of the McDonald, J.I., McGuinness, K.A., Hooper, J.N.A., 2003. Influence of re-orientation on
sponge Haliclona oculata (Porifera) with transplantation experiments. Mar. Biol. 113, alignment to flow and tissue production in a Spongia sp. (Porifera: Demospongiae:
133–143. https://doi.org/10.1007/BF00367647. Dictyoceratida). J. Exp. Mar. Biol. Ecol. 296, 13–22. https://doi.org/10.1016/
Kaandorp, J.A., Blom, J.G., Verhoef, J., Filatov, M., Postma, M., Müller, W.E.G., 2008. S0022-0981(03)00302-2.
Modelling genetic regulation of growth and form in a branching sponge. Proc. Royal McInnes, K.L., White, C.J., Haigh, I.D., Hemer, M.A., Hoeke, R.K., Holbrook, N.J.,
Soc. B: Biol. Sci. 275, 2569–2575. https://doi.org/10.1098/rspb.2008.0746. Kiem, A.S., Oliver, E.C.J., Ranasinghe, R., Walsh, K.J.E., Westra, S., Cox, R., 2016.
Kefalas, E., Castritsi-Catharios, J., Miliou, H., 2003. The impacts of scallop dredging on Natural hazards in Australia: sea level and coastal extremes. Clim. Change 139,
sponge assemblages in the Gulf of Kalloni (Aegean Sea, northeastern 69–83. https://doi.org/10.1007/s10584-016-1647-8.
27
McLean, E.L., Lasker, H.R., 2013. Height matters: position above the substratum Przeslawski, R., Alvarez, B., Battershill, C., Smith, T., 2014. Sponge biodiversity and
influences the growth of two demosponge species. Mar. Ecol. 34, 122–129. https:// ecology of the Van Diemen Rise and eastern Joseph Bonaparte Gulf, northern
doi.org/10.1111/j.1439-0485.2012.00523.x. Australia. Hydrobiologia 730, 1–6. https://doi.org/10.1007/s10750-013-1799-8.
Mendola, D., de Caralt, S., Uriz, M.J., van den End, F., van Leeuwen, J.L., Wijffels, R.H., Przeslawski, R., Alvarez, B., Kool, J., Bridge, T., Caley, M.J., Nichol, S., 2015.
2008. Environmental flow regimes for Dysidea avara sponges. Mar. Biotechnol. 10, Implications of sponge biodiversity patterns for the management of a marine reserve
622–630. https://doi.org/10.1007/s10126-008-9102-0. in northern Australia. PLoS ONE 10, e0141813. https://doi.org/10.1371/journal.
Meroz-Fine, E., Shefer, S., Ilan, M., 2005. Changes in morphology and physiology of an pone.0141813.
East Mediterranean sponge in different habitats. Mar. Biol. 147, 243–250. https:// Przeslawski, R., Alvarez de Glasby, B., Smit, N., Evans-Illidge, L., Dethmers, K., 2013.
doi.org/10.1007/s00227-004-1532-2. Benthic biota of northern Australia. Geoscience Australia SS2012t07 Post-Survey
Moore, J.A.Y., Bellchambers, L.M., Depczynski, M.R., Evans, R.D., Evans, S.N., Field, S. Report 2013/07. Canberra, Geoscience Australia, 31 pp. https://www.nespmarine.
N., Friedman, K.J., Gilmour, J.P., Holmes, T.H., Middlebrook, R., Radford, B.T., edu.au/node/1524 (accessed 15 April 2020).
Ridgway, T., Shedrawi, G., Taylor, H., Thomson, D.P., Wilson, S.K., 2012. Rakotoarivelo, T., 2019. Sponge cup garden, Sydney, Australia. You Tube AU.
Unprecedented mass bleaching and loss of coral across 12 of latitude in Western https://www.youtube.com/watch?v=Hz8XhKAAj2Q (accessed 8 March 2020).
Australia in 2010–11. PLoS ONE 7, e51807. https://doi.org/10.1371/journal. Reiswig, H.M., 1970. Porifera: sudden sperm release by tropical Demospongiae. Science
pone.0051807. 170, 538–539. https://doi.org/10.1126/science.170.3957.538.
Moran, M.J., Stephenson, P.C., 2000. Effects of otter trawling on macrobenthos and Rice, S.A., 1984. Effects of suspended sediment and burial upon survival and growth of
management of demersal scalefish fisheries on the continental shelf of north-western Eastern Gulf of Mexico corals. Manatee County Wateratlas, University of South
Australia. ICES J. Mar. Sci. 57, 510–516. https://doi.org/10.1006/jmsc.2000.0718. Florida, Sarasota, pp. 1–58. https://manatee.wateratlas.usf.edu/upload/documents/
Mote, S., Schönberg, C.H.L., Samaai, T., Gupta, V., Ingole, B., 2019. A new clionaid Effects_of_suspended.pdf.
sponge infests live corals on the west coast of India (Porifera, Demospongiae, Roberts, D.E., Davis, A.R., Cummins, S.P., 2006. Experimental manipulation of shade,
Clionaida). Syst. Biodivers. 17, 190–206. https://doi.org/10.1080/ silt, nutrients and salinity on the temperate reef sponge Cymbastela concentrica. Mar.
14772000.2018.1513430. Ecol. Prog. Ser. 307, 143–154. https://doi.org/10.3354/meps307143.
Neves, G., Omena, E., 2003. Influence of sponge morphology on the composition of the Rützler, K., 1997. The role of psammobiontic sponges in the reef community. Proc. 8th
polychaete associated fauna from Rocas Atoll, northeast Brazil. Coral Reefs 22, Int. Coral Reef Symp., Panama City, 24 – 29 June 1996, Vol. 2, 1393–1398.
123–129. https://doi.org/10.1007/s00338-003-0295-4. Sainsbury, K.J., Campbell, R.A., Whitelaw, A.W., 1993. Effects of trawling on the marine
Newcomer, K., Tracy, B.M., Chang, A.L., Ruiz, G.M., 2019. Evaluating performance of habitat on the north west shelf of Australia and implications for sustainable fisheries
photographs for marine citizen science applications. Front. Mar. Sci. 6, 336. https:// management. In: Hancock, D.A. (Ed.), Sustainable Fisheries Through Sustaining Fish
doi.org/10.3389/fmars.2019.00336. Habitat. Australian Government Publishing Service, Canberra, pp. 137–145.
Nickel, M., Donath, T., Schweikert, M., Beckmann, F., 2006. Functional morphology of Saito, V.S., Siqueira, T., Fonseca-Gessner, A.A., 2015. Should phylogenetic and
Tethya species (Porifera): 1. Quantitative 3D-analysis of Tethya wilhelma by functional diversity metrics compose macroinvertebrate multimetric indices for
synchrotron radiation-based X-ray microtomography. Zoomorphology 125, stream biomonitoring? Hydrobiologia 745, 167–179. https://doi.org/10.1007/
209–223. https://doi.org/10.1007/s00435-006-0021-1. s10750-014-2102-3.
NOAA Office of Exploration and Research, 2015. Comrades and carnivores. Sarà, M., 2002. Xenospongia Gray, 1858, In: Hooper, J.N.A., van Soest, R.W.M. (Eds.),
Transboundary Exploration of Deepwater Communities, Northern Neighbors Systema Porifera. A Guide to the Classification of Sponges. Volume 1. Kluwer
https://oceanexplorer.noaa.gov/explorations/17gulfofmaine/logs/june15/june15. Academic, Plenum Publishers, New York, Boston, Dordrecht, London, Moscow, pp.
html (accessed 25 April 2020). 264–265. https://doi.org/10.1007/978-1-4615-0747-5_1.
NOAA Office of Exploration and Research, 2016. Dive 3: We go together: commensals Santín, A., Grinyó, J., Ambroso, S., Uriz, M.J., Gori, A., Dominguez-Carrió, C., Gili, J.M.,
and parasites in the deep sea. 2016 Deepwater Exploration of the Marianas. https 2018. Sponge assemblages on the deep Mediterranean continental shelf and slope
://oceanexplorer.noaa.gov/okeanos/explorations/ex1605/logs/apr25/welcome.ht (Menorca Channel, Western Mediterranean Sea). Deep Sea Res. Part I Oceanogr. Res.
ml (accessed 1 May 2020). Papers 131, 75–86. https://doi.org/10.1016/j.dsr.2017.11.003.
NOAA Office of Exploration and Research, 2017. Dive 11: “Ridge” Seamaount. Forest of Schläppy, M.L., Hoffmann, F., Røy, H., Wijffels, R.H., Mendola, D., Sidri, M., de Beer, D.,
the weird. 2017 Laulima O Ka Moana: Exploring Deep Monument Waters Around 2007. Oxygen dynamics and flow patterns of Dysidea avara (Porifera:
Johnston Atoll. Office of Exploration and Research (accessed 15 March 2020). Demospongiae). J. Mar. Biol. Assoc. UK 87, 1677–1682. https://doi.org/10.1017/
Ocean Exploration Trust, 2017. Socorro Island sponge and coral gardens. Nautilus Live. S0025315407058146.
https://nautiluslive.org/video/2017/11/17/socorro-island-sponge-and-coral- Schmahl, G.P., 1990. Community structure and ecology of sponges associated with four
gardens (accessed 28 March 2020). southern Florida coral reefs. In: Rützler, K. (Ed.), New Perspectives in Sponge Biolog.
Orrico, V.G., 2017. Photography-based taxonomy is still really inadequate, unnecessary, Smithsonian Press, Washington D.C., pp. 376–383
and potentially harmful for biological sciences. A reply to Thorpe (2017). Bionomina Schönberg, C.H.L., 2000. Bioeroding sponges common to the Central Australian Great
12, 48–51. https://doi.org/10.11646/bionomina.12.1.5. Barrier Reef: descriptions of three new species, two new records, and additions to
Patade, P., 2019. Sea sponge & coral. Marine Life of Mumbai. https://www.marinelife two previously described species. Senckenb. Marit 30, 161–221. https://doi.org/
ofmumbai.in/photo/sea-sponge-coral/ (accessed 28 March 2020). 10.1007/BF03042965.
Patterson, M.R., Chernykh, V.I., Fialkov, V.A., Savarese, M., 1997. Trophic effects of Schönberg, C.H.L., 2001. Small-scale distribution of Great Barrier Reef bioeroding
sponge feeding within Lake Baikal’s littoral zone. 1. In situ pumping rates. Limnol. sponges in shallow water. Ophelia 55, 39–54. https://doi.org/10.1080/
Oceanogr. 42, 171–178. https://doi.org/10.4319/lo.1997.42.1.0171. 00785236.2001.10409472.
Pérez, T., Garrabou, J., Sartoretto, S., Harmelin, J.G., Francour, P., Vacelet, J., 2000. Schönberg, C.H.L., 2002a. Sponges of the ‘Cliona viridis complex’ – a key for species
Massive mortality of marine invertebrates: an unprecedented event in northwestern identification. Proc. 9th Int. Coral Reef Symp. Bali, Indonesia 2000, Vol. 1, 295–299.
Mediterranean. Compt. Rendus Acad. Sci. III Sci. Vie 323, 853–865. https://doi.org/ Schönberg, C.H.L., 2002. Pione lampa, a bioeroding sponge in a worm reef.
10.1016/s0764-4469(00)01237-3. Hydrobiologia 482, 49–68. https://doi.org/10.1023/A:1021258901538.
Petchey, O.L., Gaston, K.J., 2006. Functional diversity: back to basics and looking Schönberg, C.H.L., 2008. A history of sponge erosion: from past myths and hypotheses to
forward. Ecol. Lett. 9, 741–758. https://doi.org/10.1111/j.1461-0248.2006.00924. recent approaches. In: Wisshak, M., Tapanila, L. (Eds.), Current Developments in
x. Bioerosion. Springer, Berlin, Heidelberg, pp. 165–202. https://doi.org/10.1007/
Pitcher, C.R., Haywood, M., Hooper, J., Coles, R., Bartlett, C., Browne, M., Cannard, T., 978-3-540-77598-0_9.
Carini, G., Carter, A., Cheers, S., Chetwynd, D., Colefax, A., Cook, S., Davie, P., Ellis, Schönberg, C.H.L., 2015a. Monitoring bioeroding sponges: using rubble, quadrat, or
N., Fellegara, I., Forcey, K., Furey, M., Gledhill, D., Hendriks, P., Jacobsen, I., intercept surveys? Biol. Bull. 228, 137–155. https://doi.org/10.1086/
Johnson, J., Jones, M., Last, P., Marks, S., McLeod, I., Sheils, J., Sheppard, J., Smith, BBLv228n2p137.
G., Strickland, C., van der Geest, C., Venables, W., Wassenberg, T., Yearsley, G., Schönberg, C.H.L., 2015b. Self-cleaning surfaces in sponges. Mar. Biodiv. 45, 623–624.
2007. Mapping and Characterisation of Key Biotic and Physical Attributes of the https://doi.org/10.1007/s12526-014-0302-8.
Torres Strait Ecosystem. CSIRO/QM/QDPI CRC Torres Strait Task Final Report for Schönberg, C.H.L., 2016a. Happy relationships between marine sponges and sediments –
Cooperative Research Centre for Torres Strait Task T2.1. CSIRO Marine and a review and some observations from Australia. J. Mar. Biol. Assoc. UK 96, 493–514.
Atmospheric Research, Cleveland, 145 pp. http://www.cmar.csiro.au/datacentre/to https://doi.org/10.1017/S0025315415001411.
rres/CRCTS2003_06/pubs/T2.1_CRC-TS_Mapping_and_Characterisation_of_Torres_St Schönberg, C.H.L., 2016b. Effects of dredging on filter feeder communities, with a focus
rait_Seabed_FINAL_Report.pdf (accessed 30 March 2020). on sponges. Final report of project 6.1 of the Dredging Science Node of the Western
Plotkin, A., Gerasimova, E., Rapp, H.T., 2018. Polymastiidae (Porifera: Demospongiae) of Australian Marine. Science Institution, Perth, Western Australia, p. 127 (accessed 4
the Nordic and Siberian Seas. J. Mar. Biol. Assoc. UK 98, 1273–1335. https://doi. March 2020).
org/10.1017/S0025315417000285. Schönberg, C.H.L., Beuck, L., 2007. Where Topsent went wrong: Aka infesta a.k.a. Aka
Powell, L., 2011. Sponge abundance and the prevalence of disease on scleractinian coral labyrinthica (Demospongiae: Phloeodictyidae) and implications for other Aka spp.
in Bonaire, Dutch Caribbean. Physis J. Mar. Sci. 10, 35–39 (accessed 15 March J. Mar. Biol. Assoc. UK 87, 1459–1476. https://doi.org/10.1017/
2020). https://www.dcbd.nl/document/sponge-abundance-and-prevalence-disease- S0025315407058249.
scleractinian-coral-bonaire-dutch-caribbean. Schönberg, C.H.L., Burgess, H., 2013. Storm damage after cyclone Yasi: bioeroding
Pronzato, R., Bavestrello, G., Cerrano, C., 1998. Morpho-functional adaptations of three sponges survived. F1000 Res. 1094699 (accessed 17 March 2020). http://f1000.co
species of Spongia (Porifera, Demospongiae) from a Mediterranean vertical cliff. Bull. m/posters/browse/summary/1094699.
Mar. Sci. 63, 317–328. Schönberg, C.H.L., de Beer, D., Lawton, A., 2005. Oxygen microsensor studies on
Przeslawski, R., Ahyong, S., Byrne, M., Wörheide, G., Hutchings, P., 2008. Beyond corals zooxanthellate clionaid sponges from the Costa Brava, Mediterranean Sea. J. Phycol.
and fish: the effects of climate change on noncoral benthic invertebrates of tropical 41, 774–779. https://doi.org/10.1111/j.0022-3646.2005.04226.x.
reefs. Glob. Change Biol. 14, 2773–2795. https://doi.org/10.1111/j.1365-
2486.2008.01693.x.
28
Schönberg, C.H.L., Fromont, J., 2012. Sponge gardens of Ningaloo Reef (Carnarvon Turnbull, J. 2020. Sponges. Simple yet successful invertebrates. Flickr. https://www.
Shelf, Western Australia) are biodiversity hotspots. Hydrobiologia 687, 143–161. flickr.com/photos/johnwturnbull/albums/72157672870310525 (accessed 28
https://doi.org/10.1007/s10750-011-0863-5. March 2020).
Schönberg, C.H.L., Fromont, J., 2013. Functional sponge morphologies. The CATAMI Vacelet, J., 2006. New carnivorous sponges (Porifera, Poecilosclerida) collected from
Classification. (accessed 31 March 2020) http://catami.github.io/. manned submersibles in the deep Pacific. Zool. J. Linnean Soc. 148, 553–584.
Schönberg, C.H.L., Fromont, J., 2014. Sponge functional growth forms as a means for https://doi.org/10.1111/j.1096-3642.2006.00234.x.
classifying sponges without taxonomy. https://www.researchgate.net/publication/ Vacelet, J., 2007. Diversity and evolution of deep-sea carnivorous sponges, in Custódio,
278627643_Sponge_functional_growth_forms_as_a_means_for_classifying_sponges_ M.R., Lôbo-Hajdu, G., Hajdu, E., Muricy, G. (Eds.), Porifera Research. Biodiversity,
without_taxonomy?_sg=WvlhqKQQn6S5hfp0vmhFGe6GEU3ddgaOWa Innovation, and Sustainability. Séries Livros Museu Nacional 28, Rio de Janeiro, pp.
GrW-66PF8JE7Z5ffCOSMtQirR7yAp9kXz-gtVRW8tCeJxoNkhuAg-ffBwbp8zga 107–115.
6T4dT2D.LE0ulr_g1rVP2Ool9a5DqzcIddauehHYL-VAlgpRgUwbtAuZO2NgWh Vacelet, J., 2008. A new genus of carnivorous sponges (Porifera: Poecilosclerida,
rXOO2kvw8zv5Gll19Hm9bP2S_WcRQ2eg (accessed 28 February 2020). Cladorhizidae) from the deep NE Pacific, and remarks on the genus Neocladia.
Schönberg, C.H.L., Fromont, J., 2019. Sponge functional growth forms as a means for Zootaxa 1752, 57–65. https://doi.org/10.11646/zootaxa.1752.1.3.
classifying sponges without taxonomy. North West Atlas. (accessed 31 March 2020) Vacelet, J., 2020. Carnivorous sponges (Porifera, Cladorhizidae) from the deep South
https://northwestatlas.org/node/33141. Pacific (New Caledonia) with the description of three new species of the genus
Schönberg, C.H.L., Fromont, J., Hooper, J.N.A., Sorokin, S., Zhang, W., de Voogd, N., Abyssocladia and remarks on genus Cercicladia. Zootaxa 4767, 257–276. https://doi.
2016. New frontiers in sponge science – the 2013 Fremantle sponge conference. org/10.11646/zootaxa.4767.2.3.
J. Mar. Biol. Assoc. UK 96, 217–219. https://doi.org/10.1017/ Vacelet, J., Boury-Esnault, N., 1995. Carnivorous sponges. Nature 373, 333–335. https://
S0025315416000096. doi.org/10.1038/373333a0.
Schönberg, C.H.L., Fromont, J., Gomez, O., Alvarez, B., Battershill, C., Goudie, L., Pisera, Van Soest, R.W.M., 1989. The Indonesian sponge fauna: a status report. Neth. J. Sea Res.
A., Sorokin, S., Sutcliffe, P., Case, M., 2015. The Ningaloo Sponge Catalogue. 23, 223–230. https://doi.org/10.1016/0077-7579(89)90016-1.
Australian Institute of Marine Science Data Source. http://data.aims.gov.au/metada Van Soest, R.W.M., Boury-Esnault, N., Hooper, J.N.A., Rützler, K., de Voogd, NJ.,
taviewer/faces/view.xhtml?uuid=9eea48d8-85b5-44a0-b112-377aec2effaf Alvarez, B., Hajdu, E., Pisera, A. B., Manconi, R., Schönberg, C.H.L., Klautau, M.,
(accessed 16 April 2020). Kelly, M., Vacelet, J., Dohrmann, M., Díaz, M.C., Cárdenas, P., Carballo, J.L., Ríos,
Schönberg, C.H.L., Grass, S., Heiermann, A.T. 2006. Cliona minuscula sp. nov. P., Downey, R., Morrow, C.C., 2020. World Porifera Database. http://www.marinesp
(Hadromerida: Clionaidae) and other bioeroding sponges that only contain ecies.org/porifera/ (accessed 6 April 2020).
tylostyles. Zootaxa 1312, 1–24. 10.11646/zootaxa.1312.1. Van Soest, R.W.M., Rützler, K., 2002. Family Tetillidae Sollas, 1886, in Hooper, J.N.A.,
Schönberg, C.H.L., Lim, S.C., 2019. Psammobiosis and bioerosion: examining ecological van Soest, R.W.M. (Eds.), Systema Porifera. A Guide to the Classification of Sponges.
strategies in sponges using the case example Coelocarteria singaporensis. Facies 65, Volume 1. Kluwer Academic, Plenum Publishers, New York, Boston, Dordrecht,
14. https://doi.org/10.1007/s10347-019-0556-5. London, Moscow, pp. 85–98. https://doi.org/10.1007/978-1-4615-0747-5_8.
Schönberg, C.H.L., Tapanila, L., 2006. The bioeroding sponge Aka paratypica, a modern Vinod, K., George, R. M., Manisseri, M.K., 2009. Preliminary studies on the growth in
tracemaking analogue for the Paleozoic ichnogenus Entobia devonica. Ichnos 13, captivity of Spirastrella inconstans (Dendy) collected from the intertidal region of Palk
147–157. https://doi.org/10.1080/10420940600851552. Bay, south-east coast of India. Mar. Fish. Infor. Serv. T&E Ser. 202, 4–6. http://ep
Semeniuk, V., 1993. The Pilbara coast: a riverine coastal plain in a tropical arid setting, rints.cmfri.org.in/6438/ (accessed April 16, 2020).
northwestern Australia. Sed. Geol. 83, 235–256. Ward, T.M., Sorokin, S.J., Currie, D.R., Rogers, P.J., McLeay, L.J., 2006. Epifaunal
Short, J., Foster, T., Falter, J., Kendrick, G.A., McCulloch, M.T., 2015. Crustose coralline assemblages of the eastern Great Australian Bight: effectiveness of a benthic
algal growth, calcification and mortality following a marine heatwave in Western protection zone in representing regional biodiversity. Cont. Shelf Res. 26, 25–40.
Australia. Cont. Shelf Res. 106, 38–44. https://doi.org/10.1016/j.csr.2015.07.003. https://doi.org/10.1016/j.csr.2005.09.006.
Siebler, F., Büttner, E., Schönberg, C.H.L., Abdul Wahab, M., Brümmer, F., 2013. Effects Weissenfels, N., 1992. The filtration apparatus for food collection in freshwater sponges
of simulated dredging and trawling on Australian sponges. F1000. Research (Porifera, Spongillidae). Zoomorphology 112, 51–55. https://doi.org/10.1007/
1094793 (accessed 21 December 2020). https://f1000research.com/posters/10 BF01632994.
94793. Whitington, P., 2019. Tethya sp. golf ball sponge at Wallaga Lake, NSW. Atlas of Life in
Solé-Cava, A.M., Boury-Esnault, N., 1999. Patterns of intra- and interspecific genetic the Coastal Wilderness. https://atlasoflife.naturemapr.org/Community/Sightin
divergence in marine sponges. Mem. Queensland Mus. 44, 591–601. gs/Details/4244968 (accessed 28 March 2020).
Sorokin, S., Fromont, J., Currie, D., 2007. Demosponge biodiversity in the benthic Wilkinson, C.R., 1988. Foliose Dictyoceratida of the Australian Great Barrier Reef. II.
protection zone of the Great Australian Bight. Trans. R. Soc. S. Aust. 131, 192–204. Ecology and distribution of these prevalent sponges. Mar. Ecol. 9, 321–327. https://
https://doi.org/10.1080/03721426.2007.10887083. doi.org/10.1111/j.1439-0485.1988.tb00210.x.
Sorokin, S.J., Laperousaz, T.C., Collings, G.J., 2008. Investigator group expedition 2006: Wilkinson, C.R., Cheshire, A.C., 1989. Patterns in the distribution of sponge populations
sponges (Porifera). Trans. R. Soc. S. Aust. 132, 163–172. https://doi.org/10.1080/ across the central Great Barrier Reef. Coral Reefs 8, 127–134. https://doi.org/
03721426.2008.10887101. 10.1007/BF00338268.
Stevely, J.M., Sweat, D.E., Bert, T.M., Sim-Smith, C., Kelly, M., 2010. Sponge mortality at Wilkinson, C.R., Evans, E., 1989. Sponge distribution across Davies Reef, Great Barrier
Marathon and Long Key, Florida: patterns of species response and population Reef, relative to location, depth, and water movement. Coral Reefs 8, 1–7. https://
recovery. Proc. 63rd Gulf Caribb. Fish. Inst. 63, 384–400. doi.org/10.1007/BF00304685.
Stone, A.R., 1970. Growth and reproduction of Hymeniacidon perleve (Montagu) Wilkinson, C.R., Thompson, J.E., 1997. Experimental sponge transplantation provides
(Porifera) in Langstone Harbour Hampshire. J. Zool. 161, 443–459. https://doi.org/ information on reproduction by fragmentation. In Proc. 8th Int. Coral Reef Symp. 2,
10.1111/j.1469-7998.1970.tb02048.x. 1417–1420.
Strickland-Munro, J., Kobryn, H., Moore, S.A., Brown, G., 2016. Valuing the wild, remote Wilkinson, C.R., Vacelet, J., 1979. Transplantation of marine sponges to different
and beautiful: using public participation GIS to inform tourism planning in the conditions of light and current. J. Exp. Mar. Biol. Ecol. 37, 91–104. https://doi.org/
Kimberley, Western Australia. Int. J. Sustain. Dev. Plan. 11, 355–364. 10.1016/0022-0981(79)90028-5.
Sutcliffe, P.R., Hooper, J.N.A., Pitcher, C.R., 2010. The most common sponges on the Williams, A., Althaus, F., Dunstan, P.K., Poore, G.C., Bax, N.J., Kloser, R.J., McEnnulty, F.
Great Barrier Reef seabed, Australia, include species new to science (Phylum R., 2010. Scales of habitat heterogeneity and megabenthos biodiversity on an
Porifera). Zootaxa 2616, 1–30. https://doi.org/10.11646/zootaxa.2616.1.1. extensive Australian continental margin (100–1100 m depths). Mar. Ecol. 31,
Swierts, T., Huang, Y.M., de Voogd, N.J. 2018. The giant barrel sponge facilitates the 222–236. https://doi.org/10.1111/j.1439-0485.2009.00355.x.
recovery of coral fragments after a tropical storm in Taiwan. Coral Reefs 37, Wilson, B., Blake, S., Ryan, D., Hacker, J., 2011. Reconnaissance of species-rich coral
675–675. https://doi.org/10.1007/s00338-018-1691-0. reefs in a muddy, macro-tidal, enclosed embayment – Talbot Bay, Kimberley,
Suarez, A.V., Tsutsui, N.D., 2004. The value of museum collections for research and Western Australia. J. Royal Soc. Western Australia 94, 251.
society. Bioscience 54, 66–74. https://doi.org/10.1641/0006-3568(2004)054[0066: Wilson, S., Kendrick, A., Wilson, B., 2019. Chapter 14 – The north-western margin of
TVOMCF]2.0.CO;2. Australia. In: Sheppard, C. (Ed.), World Seas: an Environmental Evaluation. Volume
Swearingen III, D.C., Pawlik, J.R., 1998. Variability in the chemical defense of the sponge II. The Indian Ocean to the Pacific (second edition). Academic Press, London,
Chondrilla nucula against predatory reef fishes. Mar. Biol. 131, 619–627. https://doi. pp. 303–331, 10.1016/B978-0-08-100853-9.00019-1.
org/10.1007/s002270050354. Wulff, J.L., 1985. Dispersal and survival of fragments of coral reef sponges. Proc. 5th Int.
Tabachnick, K.R., 1991. Adaptation of the hexactinellid sponges to deep-sea life. In: Coral Reef Symp. Moorea, French Polynesia 5, 119–124.
Reitner, J., Keupp, H. (Eds.), Fossil and Recent Sponges. Springer, Berlin, Wulff, J.L., 1990. Patterns and processes of size change in Caribbean demosponges of
pp. 378–386. https://doi.org/10.1007/978-3-642-75656-6_30. branching morphology. In: Rützler, K. (Ed.), New Perspectives in Sponge Biology.
Thomson, D.P., Bearham, D., Graham, F., Eagle, J.V., 2011. High latitude, deeper water Smithsonian Institution Press, Washington, D. C., pp. 425–435
coral bleaching at Rottnest Island, Western Australia. Coral Reefs 30, 1107. https:// Wulff, J.L., 1991. Asexual fragmentation, genotype success and population dynamics of
doi.org/10.1007/s00338-011-0811-x. erect branching sponges. J. Exp. Mar. Biol. Ecol. 149, 227–248. https://doi.org/
Thorpe, S.E. 2017. Is photography-based taxonomy really inadequate, unnecessary, and 10.1016/0022-0981(91)90047-Z.
potentially harmful for biological sciences? A reply to Ceríaco et al. (2016). Zootaxa Wulff, J.L., 1995. Effects of a hurricane on survival and orientation of large erect coral
4226, 9. 10.11646/zootaxa.4226.3.9. reef sponges. Coral Reefs 14, 55–61. https://doi.org/10.1007/BF00304073.
Trammer, J., 1979. Some aspects of the biology of fossil solid-branching demosponges, Wulff, J.L., 1999. Rapid change and stasis in a coral reef sponge community. Mem.
exemplified by Reiswigia ramosa gen. n., sp. n., from the Lower Oxfordian of Poland. Queensland Mus. 44, 674.
Acta Geol. Pol. 29, 39–50. Wulff, J., 2001. Assessing and monitoring coral reef sponges: why and how? Bull. Mar.
Turnbull, J., 2014. Slimy lemon sponge garden- mycale mirabilis. Flickr. Accessed march Sci. 69, 831–846.
28, 2020. https://www.flickr.com/photos/johnwturnbull/14148781968/in/album Wulff, J.L., 2006a. Resistance vs recovery: morphological strategies of coral reef sponges.
-72157672870310525/. Funct. Ecol. 20, 699–708. https://www.jstor.org/stable/3806619.
29
Wulff, J.L., 2006b. Rapid diversity and abundance decline in a Caribbean coral reef Xavier, J.R., Rachello-Dolmen, P.G., Parra-Velandia, F., Schönberg, C.H.L., Breeuwer, J.
sponge community. Biol. Conserv. 127, 167–176. https://doi.org/10.1016/j. A.J., van Soest, R.W.M., 2010. Molecular evidence of cryptic speciation in the
biocon.2005.08.007. “cosmopolitan” excavating sponge Cliona celata (Porifera, Clionaidae). Mol.
Wulff, J., 2006c. A simple model of growth form-dependent recovery from disease in Phylogenet. Evol. 56, 13–20. https://doi.org/10.1016/j.ympev.2010.03.030.
coral reef sponges, and implications for monitoring. Coral Reefs 25, 415–419. Zawada, K.J.A., Madin, J.S., Baird, A.H., Bridge, T.C.L., Domelas, M., 2019.
https://doi.org/10.1007/s00338-006-0110-0. Morphological traits can track coral reef responses to the Anthropocene. Funct. Ecol.
Wulff, J., 2013. Recovery of sponges after extreme mortality events: morphological and 33, 962–975. https://doi.org/10.1111/1365-2435.13358.
taxonomic patterns in regeneration versus recruitment. Integr. Comp. Biol. 53, Zea, S., Henkel, T.P., Pawlik, J.R., 2014. The Sponge Guide: a Picture Guide to Caribbean
512–523. https://doi.org/10.1093/icb/ict059. Sponges, 3rd ed. www.spongeguide.org (accessed 22 March 2020).
30

No Taxonomy Needed Sponge Functional Morphologies Inform About

Uploaded by

Copyright:

Available Formats

No Taxonomy Needed Sponge Functional Morphologies Inform About

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

No Taxonomy Needed Sponge Functional Morphologies Inform About

Uploaded by

Copyright:

Available Formats

Ecological Indicators 129 (2021) 107806

Contents lists available at ScienceDirect