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Sea cucumbers (Echinodermata: Holothuroidea) are large and abundant members of marine benthic communities. Overexploitation worldwide has raised concern because they have important functions within ecosystems. The ecological roles of commercially exploited sea cucumbers (Aspidochirotida and Dendrochirotida) are reviewed here, focusing on recent literature. Of the more than 70 species commercially exploited, at least 12 regularly bury into sand and mud, playing major roles in bioturbation. Most aspidochirotids are deposit-feeders, reducing the organic load and redistributing surface sediments, making them bioremediators for coastal mariculture. Sea cucumbers excrete inorganic nitrogen and phosphorus, enhancing the productivity of benthic biota. This form of nutrient recycling is crucial in ecosystems in oligotrophic waters such as coral reefs. Feeding and excretion by sea cucumbers also act to increase seawater alkalinity which contributes to local buffering of ocean acidification. Sea cucumbers host more than 200 species of parasitic and commensal symbionts from seven phyla, thereby enhancing ecosystem biodiversity. They are preyed on by many taxa, thereby transferring animal tissue and nutrients (derived from detritus and microalgae) to higher trophic levels. Overexploitation of sea cucumbers is likely to decrease sediment health, reduce nutrient recycling and potential benefits of deposit-feeding to seawater chemistry, diminish biodiversity of associated symbionts, and reduce the transfer of organic matter from detritus to higher trophic levels. Ecosystem-based fisheries management needs to consider the importance of sea cucumbers in marine ecosystems and implement regulatory measures to safeguard their ecological roles.
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367
Oceanography and Marine Biology: An Annual Review, 2016, 54, 367-386
© R. N. Hughes. D. J. Hughes, I. P. Smith, and A. C. Dale, Editors
Taylor & Francis
ECOLOGICAL ROLES OF EXPLOITED SEA CUCUMBERS
STEVEN W. PURCELL1, CHANTAL CONAND2, SVEN UTHICKE3 & MARIA BYRNE4
1National Marine Science Centre, Southern Cross University, Coffs Harbour, Australia
E- mail: steven.w.purcell@gmail.com
2UMR 9220 UR CNRS IRD ENTROPIE, Université de la Réunion, Saint Denis
and Muséum National d’Histoire Naturelle, Paris, France
3Australian Institute of Marine Science, Townsville, Queensland, Australia
4School of Medical Sciences and School of Biological Sciences, F13,
University of Sydney, New South Wales 2006, Australia
Sea cucumbers (Echinodermata: Holothuroidea) are large and abundant members of marine
benthic communities. Overexploitation worldwide has raised concern because they have important
functions within ecosystems. The ecological roles of commercially exploited sea cucumbers
(Aspidochirotida and Dendrochirotida) are reviewed here, focusing on recent literature. Of the
more than 70 species commercially exploited, at least 12 regularly bury into sand and mud, playing
major roles in bioturbation. Most aspidochirotids are deposit- feeders, reducing the organic load
and redistributing surface sediments, making them bioremediators for coastal mariculture. Sea
cucumbers excrete inorganic nitrogen and phosphorus, enhancing the productivity of benthic biota.
This form of nutrient recycling is crucial in ecosystems in oligotrophic waters such as coral reefs.
Feeding and excretion by sea cucumbers also act to increase seawater alkalinity which contributes
to local buffering of ocean acidication. Sea cucumbers host more than 200 species of parasitic
and commensal symbionts from seven phyla, thereby enhancing ecosystem biodiversity. They are
preyed on by many taxa, thereby transferring animal tissue and nutrients (derived from detritus
and microalgae) to higher trophic levels. Overexploitation of sea cucumbers is likely to decrease
sediment health, reduce nutrient recycling and potential benets of deposit-feeding to seawater
chemistry, diminish biodiversity of associated symbionts, and reduce the transfer of organic matter
from detritus to higher trophic levels. Ecosystem- based sheries management needs to consider
the importance of sea cucumbers in marine ecosystems and implement regulatory measures to
safeguard their ecological roles.
Introduction
Sea cucumbers (Echinodermata: Holothuroidea) are signicant members of benthic invertebrate
communities, occurring in all of the major oceans and seas of the world. They contribute greatly to
community biomass (Birkeland 1988, Billett 1991), and their behaviours and biology have impor-
tant effects on physico- chemical processes of soft- bottom and reef ecosystems.
Commercially exploited sea cucumbers, all from the orders Aspidochi rotida and Dendrochi rotida,
provide a source of income to millions of coastal shers worldwide (Purcell etal. 2013) and a source
of nutrition to perhaps more than 1 billion Asian consumers. Presently, around 10,000 t of dried sea
cucumber is traded internationally per annum (Purcell etal. 2013), corresponding to roughly 200
million animals extracted from marine ecosystems each year. The commercial species are often
the largest of all holothuroids and can occur in high abundance in unshed habitats (Conand 1989,
368
STEVEN W. PURCELL, CHANTAL CONAND, SVEN UTHICKE & MARIA BYRNE
1990, Purcell etal. 2009, Eriksson etal. 2010). The ecology of exploited species is of special inter-
est because their natural abundance can be altered greatly by shing (Hasan 2005, Price etal. 2010,
Friedman etal. 2011). Thus, the effects on ecosystem processes and other biota are concomitantly
affected by shing.
Understanding the ecological roles of exploited species is essential for ecosystem- based sher-
ies management (EBFM), which aims to sustain healthy marine ecosystems and the sheries they
support (Food and Agriculture Organization [FAO] 2003, Pikitch etal. 2004). EBFM has become
a popular management paradigm owing to a realization that overexploitation of certain species can
trigger cascading effects on ecosystems that might diminish their ability to withstand other broad-
scale stressors. Fisheries management must take into account the likely effects of shing on other
species in the ecosystem and on ecological processes (Link 2002, Pikitch etal. 2004). An EBFM
approach requires an understanding of how exploited species are linked to other components of
the ecosystem and the inuence they have on ecosystem processes. Such an understanding helps to
devise specic regulations for key species and inform policy for responsible sheries management.
Conservation measures are also needed for more than a dozen species that have been listed as vul-
nerable or endangered with extinction (Purcell etal. 2014).
Aspidochirotid and dendrochirotid sea cucumbers occur in a vast array of habitats, from wave-
exposed zones on coral reefs to deep, soft- bottom, cold temperate habitats (Purcell et al. 2012).
They are exploited in the Pacic, Atlantic, and Indian Oceans and in the major seas, such as the
Mediterranean Sea, Caribbean Sea, Bay of Bengal, Arabian Sea, Gulf of Mexico, and North Sea
(Toral- Granda etal. 2008, Purcell etal. 2013).
Ecology and behaviours differ greatly among species. For example, some routinely bury in
sediments; others hide in reef crevices or are relatively sedentary (Purcell etal. 2012). Most of the
exploited species are deposit- feeders, gathering organic detritus and sediments from the sediment
surface (e.g., most of the aspidochirotids), and some are suspension- feeders that hold their tentacles
in the water current and trap passing phytoplankton and micro organ isms (e.g., dendrochirotids). As
a consequence of their ecological diversity, the roles that sea cucumbers play in marine ecosystems
are also varied among species.
Here, we provide a contemporary review of the ecological roles of aspidochirotid and dendro-
chirotid sea cucumbers that are exploited worldwide. We discuss the roles that the exploited holo-
thuroids play in ve main ecological arenas: contributing to sediment health; recycling nutrients;
inuencing seawater chemistry; bolstering high biodiversity through symbiotic associations; and
forming pathways of energy transfer in food chains. The review concludes with policy implications
for resource managers needing to balance these positive effects on the productivity and diversity of
the ecosystems with socio- economic pressures for shers to exploit this resource.
Maintaining and improving sediment health
Bioturbation
Bioturbation (from Latin turbatio, meaning to stir up or disturb) refers to a reworking, stirring, or
mixing of sediment layers by organisms. Bioturbation of sediments on reefs, lagoons, and seagrass
meadows has numerous physico- chemical effects on sediment permeability and water content,
chemical gradients in porewater, sediment particle composition of upper sediments, and rates of
remineralization and inorganic nutrient efux (Reise 2002, Lohrer etal. 2004). Sediment oxygen
concentrations increase through improved sediment permeability and when bioturbation pushes
lower sediments to the surface where they interact with oxygen in the water column (Solan etal.
2004). The biological consequences include enhancement of primary production, infaunal biodiver-
sity, and infaunal biomass (Solan etal. 2004).
369
ECOLOGICAL ROLES OF EXPLOITED SEA CUCUMBERS
A relatively small proportion of exploited sea cucumbers bury in sediments to bioturbate sub-
surface layers (Table1). Many of the commercially exploited sea cucumbers inhabit soft- bottom
habitats such as coral- reef lagoons, inshore seagrass meadows, mangrove systems, and deeper con-
tinental shelf habitats (Purcell etal. 2013). Some of these species bury partly or totally under the
sediment surface, sometimes on a daily cycle (Yamanouti 1939, Yamanouchi 1956, Clouse 1997,
Mercier etal. 1999). Sand and silt are pushed aside by this activity, thereby mixing surface and
subsurface sediment layers.
Burying by certain species appears to mix sediments tens of centimetres deep, and a cavity is
sometimes left by the animals (Figure1). The bioturbation action displaces at least their own body
volume in sediments (Purcell 2004). Considering that the burying species are between a few hun-
dred grams and several kilograms in weight, and potentially burying once per day, the bioturbation
effect over long timescales is likely to be substantial where they are relatively abundant. Second
to thalassinidean shrimps (Reise 2002), it appears that burying holothuroids are likely to be major
bioturbators of sediments on tropical reefs.
Deposit- feeding aspidochirotids that remain on the sediment surface disturb the upper sediment
layer through ingestion and release of faecal casts and by their locomotion across the surface. This
bioturbation activity can play an important role in redistribution of surface sediments and inuences
biotic interactions and the water- sediment interface (e.g., Uthicke 1999).
Sediment cleaning
Almost all aspidochirotid sea cucumbers are deposit- feeders on organic detritus mixed with sand
and silt in the upper few millimetres of sediments, and they defaecate sand that is generally less
organic rich than that which they consumed (Mercier etal. 1999). The ecological contribution of
deposit- feeding is important as a pathway for regeneration and mineralization of surface sediments.
Many aspidochirotid holothuroids choose organic- rich sediments and detritus from those avail-
able to them in their habitat (Hauksson 1979, Moriarty 1982, Hammond 1983, Amon & Herndl 1991,
Uthicke & Karez 1999, Slater etal. 2011), although some species appear to be rather non- selective
Table1 Commercially exploited sea cucumber species known to bury and have a signicant
bioturbation role
Species Habitat References
Actinopyga miliaris Sandy reef ats Purcell etal. (2012)
Actinopyga spinea Sandy reef ats, seagrass beds, and coral
reef lagoons
Purcell etal. (2012) (Figure1)
Anthyonidium chilensis Sandy or rocky intertidal habitats Guisado etal. (2012)
Bohadschia argus Soft sediments of reef lagoons near hard reef Purcell et al. (2016) (Figure1)
Bohadschia marmorata Silty sand in seagrass beds Yamanouti (1939, 1956), Clouse (1997)
Bohadschia vitiensis Coral reef lagoons Yamanouti (1939, 1956), Conand etal. (2010)
Holothuria arenicola Coral reef lagoons Pawson & Caycedo (1980), Hammond (1982)
Holothuria isuga Coral reef lagoons Personal observations
Holothuria lessoni Sandy reef ats, seagrass beds, and coral
reef lagoons
Conand (1990), personal observations
(Figure1)
Holothuria scabra Sandy reef ats and seagrass beds Yamanouti (1939, 1956), Conand (1990),
Mercier etal. (1999, 2000), Skewes etal.
(2000), Purcell (2004, 2010), Wolkenhauer
etal. (2010)
Holothuria spinifera Coastal sandy habitats Purcell etal. (2012)
Parastichopus regalis Sandy and rubble bottoms M. González- Wangüemert, personal
communication
370
STEVEN W. PURCELL, CHANTAL CONAND, SVEN UTHICKE & MARIA BYRNE
(Uthicke 1999, Uthicke & Karez 1999). They mostly digest bacteria, cyanobacteria, decaying plant
(e.g., seagrass and algae) matter, some diatoms, foraminiferans, fungi, and other organic matter
that constitute detritus (Yingst 1976, Moriarty 1982, Uthicke 1999, MacTavish etal. 2012). In par-
ticular, bacteria have been a commonly reported component of holothuroid diets (Moriarty 1982,
Moriarty etal. 1985, Amon & Herndl 1991). Sea cucumbers consume infauna associated with the
sediment (Moriarty 1982, Hammond 1983, Uthicke 1999), but more data are needed to determine
what they actually consume and digest. Sea cucumbers appear unable to utilize macroalgae or
seagrass (Yingst 1976), so they do not compete with macroherbivores. Stable isotope analysis of
trophic transfer would be useful to provide insights into the diet of deposit- feeding species.
Sediments defaecated by holothuroids are often lower in organic matter content than the sedi-
ments ingested, inferring that they act to ‘clean’ sediments (Amon & Herndl 1991, Mercier etal.
1999, Uthicke 1999, Michio etal. 2003, Paltzat etal. 2008, MacTavish etal. 2012, Yuan etal. 2015).
In effect, the role of sea cucumbers can be likened to that of earthworms. Gut transit of sediments
by aspidochirotid holothuroids also appears to facilitate bacterial decomposition of remaining
(refractory) organic matter in sediments (MacTavish etal. 2012). Importantly, the volume of sed-
iments ingested and defaecated per individual per year is often remarkable (9–82 kg ind–1 y–1)
(e.g., Yamanouti 1939, Bonham & Held 1963, Hammond 1982, Coulon & Jangoux 1993, Uthicke
1999, Mangion etal. 2004), so their role in cleaning sediments can be considered extensive.
AB
CD
Figure1 Bioturbation of sediments by sea cucumbers. (A) Bohadschia argus (length 40 cm) half- buried
in sediments in a coral reef lagoon (Lizard Island, Australia). (B) Holothuria lessoni (length approximately
40 cm) partly emerged from sediments on a coral reef at (New Caledonia). (C) Bohadschia vitiensis (length
approximately 35 cm) coming out of sediments in a sheltered bay (New Caledonia). Notice the large excavated
area of sediments left by the burying activity. (D) Actinopyga spinea (length approximately 30 cm) coming out
of soft sediments on a shallow reef at (New Caledonia). (Photos courtesy S.W. Purcell.)
371
ECOLOGICAL ROLES OF EXPLOITED SEA CUCUMBERS
We have heard of anecdotal accounts from shers in Papua New Guinea and Fiji that establish-
ment of cyanobacterial mats on reef sediments followed the extraction of sea cucumbers. This effect
has been found experimentally in tanks (Moriarty etal. 1985, Uthicke 1999, Michio etal. 2003).
Part of this effect may be attributed to disturbance of the upper sediments by the movement of the
sea cucumbers, which prevent the establishment of the cyanobacteria. As sea cucumbers have been
found to consume cyanobacterial mats (Uthicke 1994), this effect may be a direct consequence
of feeding.
Nutrient recycling
Recycling of organic matter has been suggested to be one of the main ecosystem functions of
holothuroids, especially in coral- reef environments where inorganic nutrients are sparse (Massin
1982, Birkeland 1988). Digestion of nitrogen- rich compounds (e.g., proteins) by holothuroids leads
to conversion of organic nitrogen into inorganic forms, which in turn can be taken up by primary
producers as nutrient sources (Figure2). Similar to most marine invertebrates, aspidochirotid holo-
thuroids excrete inorganic nitrogen as ammonium (Webb etal. 1977, Mukai etal. 1989, Uthicke
2001a). Small amounts of phosphate are also released (Uthicke 2001a). Although individual- based
rates of ammonium excretion are small, elevated values can be measured directly behind feeding
holothuroids. Based on high densities of sea cucumber populations, daily area- specic uxes of
these nutrients are high and in the range of other nutrient ux rates on coral reefs, such as nitrogen
xation, or phosphate and ammonium ux rates into the sediments (Wilkinson etal. 1984, Hansen
etal. 1987, Capone etal. 1992, Uthicke 2001a).
In coral- reef environments, it has been demonstrated that nutrients released by commercially
exploited holothuroids can increase productivity of primary producers. In aquaria and eld experi-
ments, benthic microalgal communities (microphytobenthos) had increased productivity when in
close proximity to holothuroids by receiving their waste products (Uthicke & Klumpp 1997, 1998).
Interestingly, these microalgal communities are also one of the main food sources of the holothu-
roids. Therefore, on one hand, deposit feeding reduces the microalgae and, on the other, nutrient
Feeding
Growth, respiration, reproduction
NH4+
PO4+
Excretion
Microalgae
bacteria
detritus
Uptake
Figure2 Nutrient recycling by sea cucumbers. Soluble nitrates and phosphates excreted by sea cucumbers
into surrounding seawater can be absorbed by nearby corals, macroalgae, microalgae, and bacteria. In turn,
the nutrient composition of the microalgae and bacteria is enriched, and they can be eaten by the sea cucumber
and other deposit feeders, thus forming a recycling loop in the ecosystem.
372
STEVEN W. PURCELL, CHANTAL CONAND, SVEN UTHICKE & MARIA BYRNE
release by sea cucumbers increases productivity. Uthicke (2001b) calculated that at natural holothu-
roid densities for two species studied on the Great Barrier Reef, the overall effect on the microal-
gae was positive. Thus, one can refer to the holothuroid- algae interaction as a form of gardening,
as was also suggested for lugworms (Hylleberg 1975). However, it is unclear to how many holothu-
roid species this applies. In polyculture conditions, deposit feeding of the temperate aspidochirotid
Apostichopus japonicus also converts nitrogen in particulate wastes to inorganic nitrogen, which
can be absorbed by commercially valuable macroalgae (Yuan etal. 2015). A study on another
temperate species (Australostichopus mollis) conrmed that nutrient release from holothuroids can
increase benthic productivity, although the study focused on nutrients released from interstitial
water (MacTavish etal. 2012). In that study, losses of microalgae from consumption by sea cucum-
bers outweighed the increased productivity of microalgae from nutrients they excreted.
Few other studies of holothuroid- plant interactions have been reported. One exception is a
detailed eld study investigating how overshing of a commercially important species, Holothuria
scabra (called ‘sandsh’), would affect productivity and growth of seagrass (Wolkenhauer et al.
2010). This study indicated that, in some cases, seagrass grew more slowly and biomass decreased
where H. scabra was excluded. It was assumed that, similar to the case with microalgae, seagrasses
can rapidly take up recycled ammonium and phosphate, thereby increasing productivity. Seagrasses
may also have beneted from remineralized nutrients from sea cucumber feeding or nutrients
released from the porewater in sediments because H. scabra routinely buries into sediments.
In addition to ‘full’ digestion and nutrient release, as part of the sediment ‘cleaning’ (discussed
previously) deposit- feeding holothuroids may partially digest organic matter, making it more ame-
nable to degradation by bacteria or biota on other trophic levels. For example, a Mediterranean
species (Holothuria tubulosa) feeding on seagrass detritus can facilitate increased uptake of the
detritus into the sediment (Costa etal. 2014).
Whereas most commercially exploited holothuroids are deposit- feeders, dendrochirotids such
as Cucumaria frondosa are suspension- feeders, trapping mainly phytoplankton with their tentacles
(Hamel & Mercier 1998). Little is known about nutrient recycling by these animals, but it can be
assumed that these also release ammonium as a metabolic by- product. However, high levels of urea
in body uids of a congeneric species (C. miniata) suggest that this may also be an important excre-
tion product (Jackson & Fontaine 1984).
Inuence on local water chemistry
Coral- reef ecosystems are dominated by sandy habitats composed mostly of calcium carbonate
(CaCO3) sediments from skeletons of calcifying organisms. Studies indicated that several aspido-
chirotid sea cucumber species can increase local seawater alkalinity (AT) through their digestive
processes and release of ammonia, thereby facilitating calcication by associated organisms such
as corals and calcareous algae (Schneider etal. 2011, 2013) (Figure 3). Dissolution of carbonate
sand in the sea cucumber digestive tract due to the low pH of gut uids results in production of fae-
cal casts higher in pH than the surrounding water (Hammond 1981, Schneider etal. 2011, 2013).
This, along with the release of ammonia from the sea cucumber body (Uthicke & Klumpp 1997,
Uthicke 2001a), increases the buffering capacity of surrounding seawater (Figure 3). Thus, at a
local scale, the increase in AT due to the presence of sea cucumbers might enhance the capacity of
reef organisms to calcify (Schneider etal. 2011, 2013). On the other hand, a recent experiment with
Holothuria atra indicated no overall buffering capacity of seawater alkalinity owing to production
of respiratory CO2 by H. atra (Vidal-Ramirez & Dove 2016). Effects of sea cucumbers on seawater
chemistry appears to differ considerably among species (Schneider et al. 2013) and probably oper-
ate only at local scales and where seawater ow is low. Nonetheless, the release of ammonia by
sea cucumbers potentially provides nutrients to the zooxanthellae symbionts of corals, potentially
increasing their productivity.
373
ECOLOGICAL ROLES OF EXPLOITED SEA CUCUMBERS
The presence of high- density sea cucumber populations, as characteristic of unshed reefs
(Purcell etal. 2009, Muthiga & Conand 2014, Eriksson & Byrne 2015), may be particularly impor-
tant for the integrity of reefs due to the potential of sea cucumbers to buffer changes in local carbonate
chemistry caused by ocean acidication. The increase in ocean acidication due to anthropogenic
CO2 emissions (Kleypas etal. 1999) impairs the ability of calciers to produce CaCO3 and has
resulted in a marked reduction in reef calcication (Hoegh- Guldberg etal. 2007, Death etal. 2009,
Silverman etal. 2009, Veron etal. 2009, Fabricius etal. 2014). This is a major threat to the integrity
of coral reefs and the vast diversity of species and local human communities that depend on these
ecosystems (Bellwood etal. 2004, Hoegh- Guldberg etal. 2007, Dove etal. 2013).
Research is required to further understand the contribution of different species of sea cucumbers
to sediment dissolution and the inuence of the release of respiratory CO2 by the sea cucumbers.
Such research will enable us to fully understand the contribution of sea cucumbers to community
metabolism and their potential role in increasing local AT to support reef calcication.
Symbiotic relationships
The Holothuroidea have long been recognized as having many biotic associates. Both aspidochi-
rotid and dendrochirotid commercial species tend to be relatively large as adults, with thick body
wall, and their populations can often occur at high density, yet most of the symbiosis studies have
been on aspidochirotids.
CO
2
(atm)
CO2(aq)
pH
pH
Buering
Alkalinity
NH3
Partial dissolution of carbonate sand
NH3
Figure3 Potential inuence of sea cucumbers on local water chemistry. Atmospheric (atm) CO2 dissolves
in seawater (aq, aqueous), lowering pH, a process called ocean acidication, which also lowers the satura-
tion stage of carbonate minerals (Kleypas etal. 1999, Branch etal. 2013). Carbonate sands ingested by sea
cucumbers (e.g. Stichopus herrmanni) are partially dissolved in the gut and the animals also release ammonia,
resulting in an increase in pH and total alkalinity of surrounding water (Schneider etal. 2011, 2013). Thus,
the metabolic activity of sea cucumbers may help buffer the effects of acidication at local scales and, along
with providing nutrients to promote photosynthesis of zooxanthellate (Symbiodinium) symbionts, is likely to
facilitate coral calcication.
374
STEVEN W. PURCELL, CHANTAL CONAND, SVEN UTHICKE & MARIA BYRNE
Symbionts of sea cucumbers are commensals and parasites from at least nine phyla (Jangoux
1990, Eeckhaut etal. 2004) (Table2). Parmentier and Michel (2013) recently outlined the different
symbiosis categories (parasitism, mutualism, commensalism) and the sometimes- ambiguous bound-
aries between them. This review therefore uses the classical denitions following Combes (1995):
parasites are linked to organisms by “trophic, interspecic and durable relationships”; mutualism
involves a reciprocal benet, with symbiotic mutualism implying a long- term exchange; commen-
salism refers to symbionts beneting by living on or inside their host with no reciprocal benet to
the host and includes the benet of transport (phoretism) or shelter (inquilinism) to the symbiont.
Furthering the previous syntheses by Jangoux (1990) and Eeckhaut etal. (2004), the present
review incorporates new studies published during the last decade, including some involving large
collections of holothuroids (Table2). In addition to the direct benets to the lives of the symbionts,
Table2 Organisms known to form symbiotic relationships with commercially exploited
holothuroids, listed by major taxon and symbiont genus
Symbiont major taxon Symbiont genera Host holothuroid species References
Chromista: Bacillariophyceae Cocconeiopsis Holothuria atra Riaux- Gobin & Witkowski
(2012)
Protozoa
Ciliophora Boveria, Licnophora Parastichopus californicus Eeckhaut etal. (2004)
Gregarinasina Cystobia, Diplodina,
Goniospora,
Lithocystis, Urospora
Cucumaria frondosa,
Holothuria tubulosa
Eeckhaut etal. (2004)
Acoelomorpha: Acoela Aechmalotus,
Aphanostoma,
Meara, Octocoelis
Parastichopus tremulus Jangoux (1990)
Platyhelminthes: Rhabdocoela Anoplodium,
Paranotothrix,
Wahlia, others
Actinopyga miliaris,
Australostichopus mollis,
Holothuria arenicola,
H. impatiens, H. forskali,
Stichopus herrmanni
Jangoux (1990), Eeckhaut
etal. (2004)
Annelida: Polychaeta
Polynoidae Arctonoe,
Gastrolepidia
Apostichopus japonicus,
A. parvimensis,
Australostichopus mollis,
Actinopyga echinites,
A. mauritiana, Bohadschia
argus, Holothuria atra,
H. edulis, H. leucospilota,
H. scabra, H. nobilis,
Parastichopus californicus,
Pearsonothuria graeffei,
Stichopus chloronotus,
S. herrmanni, S. horrens,
Thelenota ananas, T. anax
Cameron & Fankboner
(1989), Martin & Britayev
(1998), Britaev & Lyskin
(2002), Lyskin & Britaev
(2005), Purcell & Eriksson
(2015)
Ctenodrilidae Ctenodrilus Holothuria tubulosa Martin & Britayev (1998)
Mollusca
Bivalvia n/ i n/ i Eeckhaut etal. (2004)
Gastropoda: Opisthobranchia Plakobranchus Holothuria atra,
H. leucospilota, Thelenota
anax
Mercier & Hamel (2005)
Continued
375
ECOLOGICAL ROLES OF EXPLOITED SEA CUCUMBERS
these relationships act to increase total ecosystem biodiversity—especially in the case of obligate
relationships, where the symbiont would struggle to exist in the ecosystem without the sea cucum-
ber host.
Hosts to ectocommensals
Many ectocommensal species are known to live on commercial holothuroids, namely, those in the
Aspidochirotida. The ectocommensals belong to several phyla, and the species have generally been
only listed taxonomically in the literature. The most commonly reported are the Platyhelminthes;
the Polychaeta; the Arthropoda (copepods, crabs, and a few shrimps); and the Gastropoda (Eeckhaut
etal. 2004). ‘Piggybacking’ on the host allows the ectocommensal a refuge against predators, and
they can often feed on external food sources.
Recent studies have reported that the common Indo- Pacic Holothuria atra acts as a critical
host to discoid diatoms (Bacillariophyceae) (Riaux- Gobin & Witkowski 2012) and the opisthobranch
gastropod Plakobranchus ocellatus (Mercier & Hamel 2005). In the latter case, the sea cucumber
Table2 (Continued) Organisms known to form symbiotic relationships with commercially
exploited holothuroids, listed by major taxon and symbiont genus
Symbiont major taxon Symbiont genera Host holothuroid species References
Mollusca (Continued)
Gastropoda: Eulimidae Melanella,
Megadenus,
Enteroxenos
Actinopyga mauritiana,
Bohadschia argus,
Holothuria arenicola,
H. atra, H. cinerascens,
H. edulis, H. grisea,
H. mexicana, H. pervicax,
Isostichopus badionotus,
Parastichopus californicus,
Stichopus chloronotus,
S. herrmanni
Jangoux (1990), Cameron &
Fankboner (1989), Queiroz
etal. (2013), Eeckhaut
etal. (2004), Purcell &
Eriksson (2015)
Crustacea
Decapoda Periclimenes,
Lissocarcinus,
Hapalonotus,
Pinnotheres,
Chlorodiella
Bohadschia subrubra,
B. vitiensis, Holothuria
atra, H. fuscogilva,
H. lessoni, Holothuria
scabra, Stichopus
chloronotus, S. herrmanni,
Thelenota ananas
Jangoux (1990), Hamel etal.
(1999), Eeckhaut etal.
(2004), Lyskin & Britaev
(2005), Caulier etal. (2013,
2014), Purcell & Eriksson
(2015)
Copepoda Allantogynus,
Synaptiphilus
Actinopyga spp., Holothuria
poli, H. tubulosa
Jangoux (1990), Eeckhaut
etal. (2004)
Echinodermata
Ophiuroidea Ophiothela Stichopus chloronotus,
S. herrmanni
Purcell & Eriksson (2015)
Holothuroidea Synaptula Stichopus herrmanni Purcell & Eriksson (2015)
Actinopterygii: Carapidae Carapus, Encheliophis Bohadschia argus,
Holothuria fuscopunctata,
H. tubulosa, Isostichopus
fuscus, Parastichopus
regalis, Thelenota ananas,
T. anax
Markle & Olney (1990),
Parmentier & Das (2004),
Parmentier & Vandewalle
(2005), Parmentier etal.
(2006, 2010), González-
Wangüemert etal. (2014)
Note: n/ i, not identied.
376
STEVEN W. PURCELL, CHANTAL CONAND, SVEN UTHICKE & MARIA BYRNE
host provides the commensal with a protected spawning site and thus can be seen as crucial for its
population biology.
Both crabs and shrimps can be ectocommensals and can display intraspecic antagonism
(Lyskin & Britaev 2005), suggesting a territorial behaviour on their host sea cucumbers. The
shrimp Periclimenes imperator shows a wide variety of hosts, including 11 holothuroids (Fransen &
Hoeksema 2014). One large commercially exploited holothuroid, Stichopus herrmanni, hosts many
different epibiont species, including some echinoderms, such as ophiuroid seastars and synaptid sea
cucumbers (Figure4E,F), which do not affect the diurnal movements or the feeding rates of the host
(Purcell & Eriksson 2015).
Twelve species of pinnotherid crabs are often associated with several holothuroids, with the
Harlequin crab Lissocarcinus orbicularis (Figure4B) being a frequent symbiont (Eeckhaut etal.
2004). Caulier etal. (2014) found that sea cucumbers (eight species) are obligate hosts to these crabs
on reefs of south- western Madagascar. The crabs benet from the predator- deterrence properties of
the saponin chemicals produced by the host, which also attracts them to nd the host sea cucumbers
(Caulier etal. 2013). Research on the crabs’ diet shows that the host tissues contribute a food source,
but not an exclusive diet (Caulier etal. 2014).
Hosts to endocommensals
Endocommensals live freely in various organs and body spaces of holothuroids, but mostly in the
digestive tract where they can exit the hosts. In a similar way to the ectocommensals, they nd
effective refuge against predators. Endocommensals of sea cucumbers include species from many
ABC
DEF
Figure 4 Commensals and parasites of commercially exploited sea cucumbers. (A) Endocommensalism
by the pearlsh Carapus acus (Family Carapidae) partly emerged from the anus of Holothuria tubulosa
(Mediterranean Sea), with inset of head of the pearlsh (photos courtesy D. Bay and E. Parmentier). (B) Two
Harlequin crabs Lissocarcinus orbicularis on the body wall of Holothuria scabra (Madagascar) (photo cour-
tesy G. Caulier and I. Eeckhaut). (C) An ectocommensal scaleworm Gastrolepidia clavigera on the body wall
of Bohadschia argus (Indonesia) (photo courtesy B. Jones and M. Shimlock, Secret Sea Visions). (D) A para-
sitic snail (Family Eulimidae) on Holothuria verrucosa (La Réunion) (photo courtesy P. Bourjon). (E) Five
ectocommensal sea cucumbers Synaptula media on the outer body wall of Stichopus herrmanni (New
Caledonia) (photo: S. Purcell). (F) Numerous ectocommensal brittle stars Ophiothela cf. danae on the body
wall of Stichopus chloronotus (New Caledonia) (photo: S.W. Purcell).
377
ECOLOGICAL ROLES OF EXPLOITED SEA CUCUMBERS
different phyla, including Protozoa (gregarines, coccidias); Platyhelminthes (Acoela, numerous
Turbella ria , Rhabdocoela, and Trematoda); and nine species of shes (Table2).
Pearlshes (family Carapidae) (Markle & Olney 1990) are often cited as parasites (Jangoux
1990, Eeckhaut etal. 2004) as they can provoke small injuries or reduce gonad tissues of the holo-
thuroid hosts (Parmentier etal. 2006), but the nature of the relationship is contentious. At least nine
species are known to live in sea cucumbers in many geographical areas (Eeckhaut et al. 2004).
Pearlshes are of special interest owing to their various adaptations and the obligate nature of the
commensalisms. Sexual pairs of pearlsh can be found in sea cucumbers, which are believed to
also serve as breeding sites (González- Wangüemert etal. 2014). Using isotope analyses, Parmentier
and Das (2004) found that Carapus species probably leave their hosts to feed on external sources
(Figure4A), while Encheliophis species eat organs of their holothuroid hosts. Large commercially
exploited sea cucumbers are the preferred hosts for certain Carapus species, and it seems that
the pearlsh are often relatively uncommon among individuals in sea cucumber host populations
(C. Conand & J. Olney unpublished data, Markle & Olney 1990, Parmentier etal. 2006, González-
Wangüemert etal. 2014).
Hosts to parasites
Likewise for the commensals, parasites can be ectobiotic or endobiotic. Endoparasites most often
occur in the digestive tract and the coelomic or hemal systems of the host sea cucumbers (Jangoux
1990, Eeckhaut etal. 2004). Some umagilid atworm species (Platyhelminthes) are reported to
compete with their host for nutrients and swim in the gut or coelomic uid where they breed, so
their life- history stages rely on the sea cucumber hosts (Shinn 1983).
Numerous species of gastropods in the family Eulimidae (33 species cited by Jangoux 1990) are
ectoparasites using their proboscis to penetrate the body wall (Figure4D) and feed on the coelomic
uid, nevertheless without serious consequences to the host. The most abundant symbiont collected
by Lyskin & Britaev (2005) was the polychaete Gastrolepidia clavigera (Figure4C), which, similar
to melanellid gastropods, feeds almost exclusively on the host tissues.
As discussed, several Encheliophis pearlshes (Carapidae) feed on holothuroid tissues and are
considered parasites. They have several morphological adaptations in the jaws and teeth, supporting
their parasitic lifestyle, in which they differ from Carapus species (Parmentier etal. 2010). Similarly,
sea cucumbers are an obligate host to the pea crab, Pinnotheres halingi, which lives in the respira-
tory tree of Holothuria scabra and can be considered parasitic because it induces atrophy of the
respiratory tree (Hamel etal. 1999). Holothuria atra is a host for parasitic entochonchid gastropods
(M. Byrne personal observations). These bizarre parasites enter the sea cucumber as a larva, attach
to the digestive tract, and then grow into a spiral vermiform structure that forms a brood chamber
for the developing young, which leave the holothuroid host through the anus (Byrne 1985b).
Value to food chains
A sacricial role played by sea cucumbers is to act as prey to predator species, thereby transferring
energy from microalgae and organic detritus to consumers at higher trophic levels. Many of the
predators themselves are shed by humans. Although sea cucumbers have chemical defences (e.g.,
saponins, terpenes) and sticky Cuvierian tubules to deter predators (Stonik etal. 1999, Hamel &
Mercier 2000, Van Dyck etal. 2009, 2011), they are known to be consumed by diverse predators
from at least seven phyla (Table3) (also see Francour 1997). Sea cucumbers are known to be eaten
by at least 19 species of seastar, 17 species of crustaceans, several gastropods, and around 30 species
of shes (Francour 1997, Dance etal. 2003).
In temperate regions, certain species of seastars are major predators of aspidochirotid and den-
drochirotid sea cucumbers (Jangoux 1982, Yu etal. 2015). Some seastars in the genus Solaster
378
STEVEN W. PURCELL, CHANTAL CONAND, SVEN UTHICKE & MARIA BYRNE
appear to specialize their feeding on non- commercial sea cucumber species and can induce evis-
ceration and consume the released organs (Byrne 1985a). Solaster endeca is the main predator of
the dendrochirotid Cucumaria frondosa (So etal. 2010). Temperate sea cucumbers are also eaten by
marine mammals of high trophic levels, such as sea otters (Enhydra lutris). Although the sea otters
typically eat other prey such as sea urchins and bivalves, the aspidochirotid Parastichopus califor-
nicus is easy prey, and its populations declined dramatically some decades after the introduction of
Table3 Predators of commercially exploited sea cucumber species
Predator major taxon Prey holothuroid species References
Annelida: Polychaeta Cucumaria frondosa Medeiros- Bergen & Miles (1997)
Crustacea
Copepoda Apostichopus japonicus (larvae) Yu etal. (2015)
Decapoda Cucumaria miniata Francour (1997)
Psolus chitonoides Francour (1997)
Holothuria scabra Purcell & Simutoga (2008), Lavitra etal.
(2009), Robinson & Pascal (2012)
Apostichopus japonicus Yu etal. (2014, 2015)
Holothuria scabra (in captivity) Pitt etal. (2004), Bell etal. (2007)
Stichopus tremulus Francour (1997)
Parastichopus californicus Francour (1997)
Gastropoda
Tonnidae Various species Francour (1997)
Columbellidae Psolus chitonoides Francour (1997)
Ranellidae Apostichopus japonicus, Bohadschia argus Conand (1994), Kyoung & Jae (2004)
Asteroidea Various species Francour (1997)
Holothuria scabra Purcell & Simutoga (2008)
Cucumaria frondosa So etal. (2010)
Apostichopus japonicus Hatanaka etal. (1994), Yu etal. (2014, 2015)
Australostichopus mollis Slater & Jeffs (2010)
Parastichopus californicus Cameron & Fankboner (1989)
Pices
Elasmobranchii Stichopus chloronotus Francour (1997)
Actinopterygii
Balistidae Holothuria scabra Dance etal. (2003)
Labridae Holothuria scabra Francour (1997), Dance etal. (2003)
Lethrinidae Holothuria scabra Dance etal. (2003)
Nemipteridae Holothuria scabra Dance etal. (2003)
Sparidae Cucumaria sp. Francour (1997)
Gadidae Stichopus tremulus Francour (1997)
Parastichopus californicus Francour (1997)
Hexagrammidae Cucumaria spp. Francour (1997)
Pinguipedidae Australostichopus mollis Francour (1997)
Sebastidae Apostichopus japonicus Yu etal. (2014)
Reptilia: Cheloniidae Holothuria scabra Reports from shers, S.W. Purcell personal
communication
Mammalia
Phocidae Thyonidium sp. Francour (1997)
Mustelidae Parastichopus californicus Larson etal. (2013)
Odobenidae Several species Francour (1997)
379
ECOLOGICAL ROLES OF EXPLOITED SEA CUCUMBERS
sea otters in south- eastern Alaska (Larson etal. 2013). Therefore, sea cucumbers can be signicant
food sources for multiple trophic levels.
In tropical regions, a wide range of benthic invertebrates and shes avidly consume sea cucum-
bers (Table3). For example, large gastropods such as Tonna perdix prey on sea cucumbers, engulf-
ing them with their large exible siphon (Bourjon & Vasquez 2016). Sea cucumbers are also eaten
by Triton snails (Conand 1994, Kyoung & Jae 2004), which themselves have been threatened by
shell collectors. Predation by shes is considered to be minor (Francour 1997), but shes can swal-
low juvenile sea cucumbers whole (Dance etal. 2003), so their predation impact might be signi-
cant in some areas.
In some instances, sea cucumbers offer their internal organs to the predator, through stress-
induced evisceration, in place of being killed. Stichopus species can also shed parts of their body
wall in an effort to distract a predator (Kropp 1982). Hence, sea cucumbers may infrequently pass
on parts of their body tissue to higher trophic levels.
The literature shows that sea cucumbers and their tissues transfer energy to a high number of
both benthic (e.g., crabs, gastropods, and seastars) and benthopelagic predator species (e.g., mam-
mals and shes), and it is difcult to gauge which groups are most signicant in sea cucumber
predation globally. Dendrochirotid sea cucumbers use suspension- feeding, thereby contributing to
pelagic- benthic coupling by taking phytoplankton and occasional zooplankton from the water col-
umn and transforming the matter into benthic animal tissue (Hamel & Mercier 1998). Clearly, sea
cucumbers present a signicant pathway by which energy and nutrients from detritus and plankton
can be transferred to benthic and benthopelagic food webs.
Policy implications
The broad roles that exploited sea cucumbers play in ecosystems are promoting habitat health,
amplifying biodiversity, and supporting productive food chains. In more specic terms, the services
they provide are improving sediment quality, water chemistry, and nutrient recycling, which benet
ecosystem health and productivity; increasing species richness through symbioses with smaller
parasitic and commensal organisms; and forming a substantive link in the transfer of energy in
deposited detritus and microalgae to higher trophic levels in marine food webs.
The accumulation of waste products from uneaten food, faeces, and pseudofaeces on the seabed
in coastal mariculture operations is an environmental concern (Paltzat etal. 2008). Sediment bio-
remediation is valued because commercially exploited sea cucumbers have the potential to reduce
waste loading and offer additional, high- value, harvestable seafood. Waste organic matter in sedi-
ments underlying farmed shellsh can be reduced by the aspidochirotes Australostichopus mollis
(Slater & Carton 2009, MacTavish etal. 2012, Zamora & Jeffs 2012), Parastichopus californicus
(Paltzat et al. 2008), and Apostichopus japonicus (Zhou et al. 2006, Yuan et al. 2015). Hence,
there is opportunity to take advantage of the sediment- cleaning role of sea cucumbers in modied
coastal habitats.
For predators that rely heavily on sea cucumbers as a major food source, depletion of sea cucum-
ber populations through shing is likely to have a negative impact. For example, the seastar Solaster
endeca is known to be more abundant where their prey sea cucumber Cucumaria frondosa is also
abundant (So etal. 2010). Thus, overexploitation of sea cucumbers may result in a loss of biodiver-
sity or abundance of these predator species or cause them to switch to other prey species, potentially
resulting in cascading effects in the ecosystem.
Sustainable exploitation of dense sea cucumber populations may be possible if investments are
made to determine commercially viable stocks and manage shing to within modest and sustain-
able limits. Unfortunately, history shows that such prudent management is rarely applied (Purcell
etal. 2013). Populations of exploitable species are often shed to critically low levels at which they
struggle to repopulate naturally (Bell etal. 2008, Friedman etal. 2011) and probably cease to make
380
STEVEN W. PURCELL, CHANTAL CONAND, SVEN UTHICKE & MARIA BYRNE
signicant contributions to ecosystems. Population declines over broad geographic ranges were suf-
ciently serious to result in the listing of 13 holothuroid species as vulnerable or endangered with
extinction (Purcell etal. 2014). Exploitation by shing may have a cascading impact on biodiversity
because depletions in host sea cucumber populations will also deplete symbiont populations (see
Table2).
This review suggests that large- scale depletions through excessive shing are likely to have
indirect effects on the productivity and diversity of soft- bottom habitats such as seagrass beds and
coral- reef lagoons. Fishery management should be especially conservative on coral reefs because it
is in these carbonate- rich habitats that sea cucumbers can most affect ocean chemistry. Coral reefs
are in decline globally from the impacts of a range of broadscale stressors (Hoegh- Guldberg 1999,
Pandol etal. 2003, Bellwood etal. 2004, Hoegh- Guldberg etal. 2007). The changes to local water
chemistry and nutrient availability by the feeding activities of sea cucumbers offer tangible contri-
butions to coral- reef resilience. However, the potential enhancement of reef calcication through
the inuence of sea cucumbers on water chemistry is only likely to be effective in areas that are not
highly ushed, where the sea cucumbers are in high densities and where they live in close associa-
tion with coral, as is the case for Stichopus herrmanni (Figure3) in the unshed lagoon system
investigated by Schneider etal. (2011, 2013).
Fishery management espousing EBFM principles must take into account the ecosystem services
provided by sea cucumbers. For example, species- specic bans or catch limits could be imposed to
limit shing of some of the burying species (Table1), as these are most important in bioturbation
of sediments. Many nsh sheries target species that feed on soft- bottom invertebrates, so it is
conceivable that sheries productivity could decline as a consequence of depletions in sea cucum-
ber populations. Some sea cucumber species may warrant specic protection if they are especially
important in coastal and offshore food chains. Research to further understand their predators, and
the importance of sea cucumbers to their diets, would help resource managers to better evaluate
the potential ecosystem benets from stricter regulatory measures on shing sea cucumbers. Some
exploited species, such as Holothuria atra, have a low commercial value to shers and can occur in
high densities and process great quantities of sand and detritus (Uthicke 1999). Another ecosystem-
based policy could be to exclude low- value species from the lists of permissible species to be har-
vested because the nancial return for shers and exporters is relatively low but they still have an
important value to the ecosystem.
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... Sea cucumbers (Holothuroidea) feed on the organic detritus mixed with sand/silt and may be recognized by their cucumber-shaped body elongated along the oral/aboral axis. Species of the genus Holothuria are known to host various organisms including annelids, mollusks, crustaceans, and fish [9,10]. The harlequin crab, Lissocarcinus orbicularis (Dana, 1852), is an example of a symbiont crab that associates with sea cucumbers, typically seeking refuge on large holothuroid species [11]. ...
... One of the best known associations dates back to almost two centuries ago, when Quoy and Gaimard made the first observations concerning pearlfish (Ophidiiformes: Carapidae) and sea cucumbers, during the voyages of the French research vessel l'Astrolabe [10,13]. These species of the genus Carapus Rafinesque, 1810 and Encheliophis Müller, 1842, present a singular lifestyle using the coelomic cavity of sea cucumbers as shelter [13][14][15]. ...
... This shows that these juvenile sparids can forage in the same locations where they find refuge. This way, in addition to protection, we can raise the hypothesis that the bioturbation of sediments performed by sea cucumbers [10] could also expose potential prey and benefit the young fish. The limited natural habitat complexity on soft bottoms compared to reef ecosystems and structurally complex benthic organisms (e.g., cnidarians) [4,5], may favor inter-and intra-specific relationships of structurally complex organisms with low mobility, as in this case. ...
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During a diving survey on soft-bottom habitats in the Gulf of Cadiz (Southwestern Spain), the use of the sea cucumber Holothuria arguinensis (Echinodermata, Holothuriidae) as a shelter by juvenile Senegal’s sea bream Diplodus bellottii (Chordata: Sparidae) was observed. Eight juvenile sea bream D. bellottii were videoed sheltering under the sea cucumber’s body. This observation highlights the importance of sea cucumbers as a shelter for juvenile fish, providing a microhabitat to take refuge from predators. This is the first report of juvenile sea bream sheltered by a sea cucumber.
... Echinoderms, a well-defined and highly-derived clade of metazoans with approximately 7,000 species, can be found in various habitats ranging from shallow intertidal areas to abyssal depths [13]. Numerous echinoderms have been found with diverse macrosymbiotic organisms, including feather stars (crinoids) [14][15][16], sea cucumbers (reviewed by Martin & Britayev [17]; Purcell et al. [18]), sea urchins [15,16,[19][20][21], brittle stars [17], and starfish [17,19], as well as the small crustacean copepod associated with brittle stars [22]. Approximately 1,500 species of starfish live in all marine waters [23], and 48 valid species from 10 families have been recorded in waters around Taiwan [24,25]. ...
... Several reports have indicated the presence of several mollusks in the shallow waters of hydrothermal vent areas on the eastern side of Kueishan Island, but not M. martinii [5,6,71]. Among holothurian symbionts, sea snails in the genus Melanella are parasites [18,[72][73][74]. Most of them attach to the hosts' skin, piercing through the tissue with their specialized proboscis and feeding on coelomocytes. ...
... Most of them attach to the hosts' skin, piercing through the tissue with their specialized proboscis and feeding on coelomocytes. These attachment strategies do not have severe effects on the hosts [18,72]. However, in this study, M. martinii was associated with starfish, an unusual host in the genus Melanella. ...
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During an investigation program of faunal diversity in the shallow reef zone of the active volcanic island off northeastern Taiwan in July and September 2020, numerous individuals of the starfish Echinaster luzonicus (Gray, 1840) were found, and some individuals were found with associated symbionts. Starfish sampling in the 150-m coral reef zone was undertaken at a depth of 8 m through scuba diving. For each type of potential macrosymbiont, both the dorsal and ventral sides were carefully examined. The prevalence of macrosymbionts on the starfish E . luzonicus was recorded. The most common symbiotic organism on E . luzonicus was the ectoparasitic snail Melanella martinii (A. Adams in Sowerby, 1854), followed by the pontoniine shrimp Zenopontonia soror (Nobili, 1904) and the rare polychaete scaleworm Asterophilia carlae Hanley, 1989. The prevalence ratio with host E . luzonicus was low and varied by 8.62% and 4.35%, 6.03% and 0%, and 0.86% and 0.72% in July and September 2020 for M . martinii , Z . soror , and A . carlae , respectively. The present study is the first to discover the scaleworm A . carlae as a macrosymbiont of the tropical starfish E . luzonicus , with a widespread distribution, off Taiwan’s northeastern coast, an area influenced by the Kuroshio Current.
... Sea cucumbers are abundant in coral-reef coastline benthic communities (Bakus, 1973). Most sea cucumber species in these areas feed on small benthic particulate matter and have a significant role as bioturbators (Purcell et al., 2016;Wolkenhauer et al., 2010) and are thus ecologically important. Via their feeding activity, sea cucumbers enhance the productivity of their surrounding ecosystems (Uthicke & Klumpp, 1998;MacTavish et al., 2012;Wolkenhauer et al., 2010). ...
... Furthermore, sea cucumbers are even suggested to be crucial for buffering local ocean acidification by increasing the pH through ammonia discharge (Uthicke, 2001a;Schneider et al., 2011Schneider et al., , 2013. Finally, sea cucumbers often host many symbiotic species (Purcell et al., 2016;Eeckhaut et al., 2004;Hamamoto & Reimer, in press) and hence contribute to local marine biodiversity. ...
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Sea cucumbers are important ecological engineers in marine ecosystems. However, the fishery demand of some species, especially large-epifaunal and commercially used (LEC) sea cucumbers, has risen drastically, resulting in serious depletion of local populations for many species. Despite this problem, basic ecological data on sea cucumbers, such as population densities and preferred habitats, are often still insufficient. Here, we report on the population densities of multiple LEC sea cucumber species, and their ambient benthic communities at eight sites around Okinawa Islands. Further, we discuss the correspondence between sea cucumber densities and the surrounding coral communities. Our results show two sites within national or quasi-national parks, Aka and Manza, where stricter rules have been placed on fisheries and land reclamation compared to other areas, had the highest and third highest sea cucumber population densities among sites, respectively. Holothuria atra was observed at all survey sites and made up the majority of sea cucumber populations at all sites except for Chatan and Sesoko, where Holothuria leucospilota and Stichopus chloronotus were most abundant, respectively. Regarding the relationships between benthic composition and LEC sea cucumber species, S. chloronotus was significantly correlated with dead corals, scleractinian corals, and coralline algae. As well, H . leucospilota had significant correlations with rubble. Although there were no significant correlations between any specific scleractinian coral genus and sea cucumber densities, S. chloronotus was marginally insignificant with Platygyra and Psammocora . Notably, medium- to highly valued species were sparse in our surveys, and most of them appeared at only one site. Additionally, at one site (Odo), only three LEC sea cucumber individuals were observed. Combining these facts with relatively low population densities around the Okinawa Islands compared to densities reported in previous research from the Indo-West Pacific Ocean region, we conclude that Okinawan LEC sea cucumber populations have been and are being impacted by high levels of direct ( e.g ., overexploitation, as well as coastal development) and indirect anthropogenic pressure ( e.g ., decreasing water quality). To address the current situation, repeated monitoring and more detailed investigations to reveal the drivers that determine LEC sea cucumber species aggregations and population densities are urgently needed, along with more robust management of remaining LEC sea cucumber populations.
... In particular, they are significant members of tropical and subtropical shallow water ecosystems as they often show high population densities and process large amounts of sand through their feeding behavior (Uthicke 1999). Holothurians have many ecological roles that are crucial for coral reef ecosystems (Purcell et al. 2016), and among them, hosting associating creatures is important in maintaining biodiversity (Eeckhaut et al. 2004). Holothurians are known as hosts of multiple taxa, both epizoically and endozoically (e.g. ...
Article
Photograph records of four holothurian individuals upon which colonial ascidians were associated epizoically are reported from the waters around Akajima Island, Kerama Islands, Okinawa, Japan. Although holothurians are known to be hosts of many organisms, these new observations add a new perspective to understanding the ecological role of holothurians as mobile scaffolds. Some ascidians have limited capabilities of locomotion, but we believe an association with holothurians would increase the mobility of ascidians. On the other hand, such associations may be beneficial as part of the holothurians’ chemical defenses, since some ascidians and/or harbored cyanobacteria produce bioactive compounds. Even though these observed cases may be temporary associations, it is apparent holothurians are ecosystem engineers on coral reefs not only due to their feeding behavior, but also due to their associated fauna.
... Echinoderms are also ecologically important. Sea cucumbers, for example, make important contributions to nutrient cycling and energy transfer (Purcell et al. 2016). Other DOI: 10.1201/9781003288602-9 echinoderms have been shown to be important ecosystem engineers (Lessios et al. 1984, Carpenter 1985 and/or keystone species (Paine 1969, Hughes et al. 1985, Ling et al. 2015, Menge et al. 2016. ...
Chapter
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Echinoderms are a common component of benthic marine ecosystems, with many being ecologically and/or economically important. Like many marine organisms, most echinoderms have a bipartite life history with a planktonic larval phase and a benthic adult phase. The transition between these phases (i.e. settlement) is complex and comprises a cascade of events including the location, exploration and selection of suitable benthic habitat, and metamorphosis to adapt from a pelagic to a benthic lifestyle. This review provides a comprehensive synthesis of the various processes involved in the settlement phase across all five extant classes of echinoderms. Central to the review is a detailed assessment of settlement behaviour and the diverse mechanisms of settlement induction. Most echinoderms, including keystone sea urchins, starfishes and sea cucumbers, do not settle indiscriminately; specific environmental conditions or cues are often necessary for settlement to occur, resulting in marked spatial and temporal variability in settlement rates. Fluctuations in settlement, in turn, lead to major changes in the local abundance of echinoderms and often have profound ecological consequences, due to the pivotal role that many echinoderms play in ecosystem functioning. Given important knowledge gaps persist, this review also explores opportunities for future research to advance our understanding of this critical early life-history phase.
... Holothurians, known as sea cucumbers, are common benthic marine invertebrates belonging to the Phylum Echinodermata, Class Holothurioidea, represented by more than 1500 species worldwide (Horton et al., 2018). Most sea cucumbers are strong deposit-feeder bioturbators and, as such, are thought to play a key ecological role in benthic biogeochemistry (Roberts et al., 2000;Uthicke, 2001;Mangion et al., 2004;Amaro et al., 2010;Purcell et al., 2016;Neofitou et al., 2019). ...
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Holothuria tubulosa is one of the most common sea cucumber species inhabiting the Mediterranean Sea. Due to its commercial interest for the international market, it has been harvested without proper management causing the overexploitation of its stocks. Inadequate management is also caused by lack of information on basic biology and ecology not allowing the estimating of the species vulnerability and resilience to growing anthropogenic pressures. In this paper, we have investigated basic life-history traits of H. tubulosa (population structure and reproductive cycle) in a population of Central-Western Mediterranean (Sardinia, Italy). A macroscopic maturity scale for both sexes was defined through an instrumental colorimetric analysis of the gonads and the ramification level of the gonad's tubules, subsequently confirmed by histological analysis. The seasonal trend of the Gonado-Somatic Index, the changes in color of the gonads and tubules ramification indicated that the spawning period of H. tubulosa was concentrated in summer with a peak in late August, closely related to the increase in water temperature. A synchronous development of the gonads, with a unique and short reproductive event during the year, was also detected. In conclusion, this study provides new evidence on the biological and ecological features of H. tubulosa, essential data for developing a scientifically-based stock assessment as well as conservative management at a local scale. Finally, we provided basic information for the domestication of broodstock in a conservative hatchery.
... Overexploitation of sea cucumbers has raised concerns because these organisms are important for ecological functions in the marine ecosystems as deposit-feeders by reducing the organic load and redistributing surface sediments [42]. Adopting proper management measures, such as fishery quotas, which are commonly undermined by the IUU fishing, may lead to severe depletion or even collapse of the fishery. ...
Article
Between 2010 and 2018, the sea cucumber fishing in the Campeche Bank, Mexico, was a flourishing fishery showing increasing landings followed by a precipitous decline, where illegal, unreported, and unregulated fishing (IUU) was an important factor to its deterioration. Currently, despite this fishery is under permanent fishing ban since 2019, the IUU fishing prevails. This work aims to reconstruct the past sea cucumber catch, and species composition, in this region based on seizures analyses, between 2010 and 2021, collected from official documents. We estimated the total IUU catch of sea cucumber at 8117.6 t and detected that fishery statistics, based on the sea cucumber fishery in the southern Gulf of Mexico reported to FAO, have information gaps indicating overexploitation of Isostichopus badionotus. Our current assessment must be used cautiously, and may serve to justify the need to conduct these analyses in order to understand the reality of IUU fishing in the region. We recommend incorporating fishers’ community programs in order to deter the IUU fishing through active participation of legal fishing dealers, in agreement with fisher cooperatives or guilds, which are eager to support the sea cucumber fishery in the Yucatan and also implementing fishing refuge areas (FRAs) for the development of guided and supervised stock restoration campaigns.
... Holothurians, commonly known as sea cucumbers, are important shery species in many parts of the world. There are about 70 species, which are commercially harvested for the dried sea cucumber, 'trepang' or 'beche-de-mer' market (Purcell et al. 2016). International trade is rapidly increasing both in diversity and scale, which has been recorded in at least 70 countries (Louw and Bűrgener 2020). ...
Preprint
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Commercially available microalgae concentrates used in the culture of Holothuria scabra were compared to live microalgae. Larvae were reared under a fixed daily feeding ration of 20,000 cells mL − 1 using three commercial concentrates (Instant Algae®, Reed Mariculture Inc.): TW 1200 ( Thalassiosira weisflogii ; TW), TISO 1800 ( Isochrysis sp.; TISO), and Shellfish 1800 (mixed diatom; SHELL) and compared with live Chaetoceros calcitrans (CC). The efficacy of diets was evaluated based on larval growth, development, and survival to late auricularia (LA) with hyaline spheres (HS) and post settled juveniles. The average size in TISO (855.7 ± 62.67µm) was significantly higher compared with SHELL. In contrast, larvae in TW did not progress beyond middle LA. Development was much better in CC compared to all the microalgal concentrates. Larvae fed CC reached LA stage earlier, attained significantly larger sizes (1028.43 ± 19.38 µm), and have significantly higher incidence and size of HS. Better metamorphic and settlement performance of larvae in CC and SHELL treatment maybe related to the higher carbohydrate content in these feeds. Average post settled juveniles in CC (9,268 ± 2,183.79) were over three times more in SHELL, and an order of magnitude for TISO. Higher costs per juvenile can be largely attributed to the low post settled juvenile yield and longer feeding duration when using microalgae concentrates. The estimated cost of producing each juvenile using SHELL is $0.036 and $0.210 for TISO, compared to $0.009 per juvenile using CC. Opportunities to optimize the use of microalgal concentrates as supplemental feeds are discussed.
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The main goal of this study was to investigate the seasonal contaminants changes of three sea cucumber species caught from the Northeast Atlantic. The risk associated with the consumption of these target species taking into account the consumers age group was also evaluated. For this, was analysed the concentration of Cd, Pb and Hg during spring, summer, autumn and winter in two different tissues (body wall and muscle band) of female and male. Average concentration of the Cd, Pb and Hg were different between species, significant differences were also observed considering sex and tissue factors. Unlike, the seasons do not seem to interfere in the concentration of these elements. In general, Holothuria arguinensis (Cd < 0.03 mg kg − 1 ; Pb < 1.20 mg kg − 1 ; Hg < 0.03 mg kg − 1 ), Holothuria forskali (Cd < 0.03 mg kg − 1 ; Pb < LoD; Hg < 0.02 mg kg − 1 ) and Holothuria mammata (Cd < 0.04 mg kg − 1 ; Pb < 0.56 mg kg − 1 ; Hg < 0.047 mg kg − 1 ) showed levels lower than those regulated by European Union (Cd 0.05 mg kg − 1 ; Pb 0.5 mg kg − 1 ; Hg 0.5 mg kg − 1 ). The risk associated with the consumption of these species is low since the amount that can be consumed by adults, based on the maximum concentrations of each element, is high. As it is scarce or does not exist, these data may allow contribute for a data basis for future elaboration of new regulations limiting the maximum concentrations of metals in the consumption of echinoderms.
Article
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Tropical sea cucumbers are among the largest mobile invertebrates on coral reefs and are widely regarded as sedentary. Mark-recapture methods provide empirical estimates of movement and growth but have often been unsuccessful with sea cucumbers. We applied a new photographic mark-recapture technique to measure rates of short-term displacement (over a few days), long-term displacement (over 2 yr) and growth of Bohadschia argus and Thelenota ananas on the Great Barrier Reef, Australia. Recapture rates were 50–100% in the short-term study and 50–77% in the long-term study. In the short-term studies in 2010 and 2012, average movement rates ranged 2–8 m d−1 for B. argus and 5–9 m d−1 for T. ananas. Long-term movement averaged 15–47 m over 2 yr, with some individuals displacing less than 5 m and several others moving more than 100 m. Our study shows that some tropical sea cucumbers can be highly mobile, and many appear to display home ranging. Growth rates were positive yet modest for smaller individuals, but many of the large individuals lost weight over the 2 yr study. Classical growth models indicated that B. argus attain an average maximum size in 15–20 yr, and the empirical data on growth show that they can lose or gain weight thereafter. Hence, longevity appears to be at least several decades. The 2 species are slow growing, and the negative growth in large individuals undermines previous estimates of growth and longevity based on size-frequency data.
Book
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Sea cucumbers are exploited and traded in more than 70 countries worldwide. This book provides identification information on 58 species of sea cucumbers that are commonly exploited in artisanal and industrial fisheries around the world. Not all exploited species are included. It is intended for fishery managers, scientists, trade officers and industry workers. This book gives key information to enable species to be distinguished from each other, both in the live and processed (dried) forms. Where available for each species, the following information has been included: nomenclature together with FAO names and known common names used in different countries and regions; scientific illustrations of the body and ossicles; descriptions of ossicles present in different body parts; a colour photograph of live and dried specimens; basic information on size, habitat, biology, fisheries, human consumption, market value and trade; geographic distribution maps. The volume is fully indexed and contains an introduction, a glossary, and a dedicated bibliography.
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The feeding of the epibenthic deposit-feeder Hoforhuria rubulosa GhlELlN and its intlucncc on sediment metabolism was investigatcd from February 1988 to February 1989. Water sarnptcs, specimens of H. rubulosu. and samples of freshly egested fcccs were taken by SCUBA diving in a 5 rn deep seagrass bed at the Island of Ischia in the Gulf of Naples (Italy). Particulate organic carbon (POC), particulate organic nitrogen (PON), total particulate carbohydrates (PCHO). and bacterial biomass exhibited higher values in the foregut than in the surrounding sediment. Even the frcshly egested feces were richer in the organic components than the sediment. Thc percentage of growing bacterial cells increased from 4.1 % in the sediment to 12.2 % in the foregut and declined to 1 I .6 % in the hindgut and 6.2 % in freshly egested feces. On an annual average. absorption efficiency was highest for bactcria (X = 71 %); for PON we calculated a mean absorption efficiency of 20.9 %, for PCHO 19.5 %. It was cstirnated that bactcrial biomass supplied between 4 and 25 % of the respiratory carbon demand of H. rubulosa. We present evidence that the feeding activity of H. tubufosu stabilizes the bacterial community in the sediment. Furthermore. our data indicate that H. rubulosu reacts quickly to changing conditions, such as sedimented phytoplankton blooms.