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Abstract

This article presents the results from the assessment of sea cucumbers in the order Aspidochirotida for the International Union for Conservation of Nature (IUCN) Red List of threatened species. The results were published by IUCN in June 2013. Of 377 species examined, 16 were classified as threatened with extinction (7 as endangered, 9 as vulnerable) based on standard IUCN methodology. We also summarise findings from a recent publication about the drivers of extinction risk in these sea cucumbers. The IUCN listing sends a stern message to resource managers for the conservation of threatened species. The IUCN Red List may also serve to guide future evaluation by CITES (the Convention on International Trade in Endangered Species of Wild Fauna and Flora) for listing some of the species on Appendix II or III in order to set conditions on the trade of those species. We discuss some issues of CITES listing for the Philippines, as a “hotspot” country, and recommend that sea cucumbers should be re-evaluated for listing on CITES Appendix II and III.
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SPC Beche-de-mer Information Bulletin #34 – May 2014
Introduction
Sea cucumbers were once considered a marginal
invertebrate marine resource and only recently
shown to be significant to global trade, livelihoods
and marine ecosystems. Correspondingly, they
have been the subject of increased worldwide
interest for scientific knowledge, sustainable use
and conservation purposes (Lovatelli et al. 2004;
Bruckner 2006; Toral-Granda et al. 2008; Purcell et
al. 2013).
Unlike the Convention on International Trade
in Endangered Species of Wild Fauna and Flora
(CITES), the International Union for Conservation
of Nature (IUCN) Red List is not a multilateral
political agreement and does not impose trade
or other conservation conditions on countries
and states. However, the scientific process of
conducting standardised and systematic species
extinction risk assessments for the IUCN Red List
is often subsequently used as an information tool
for conservation planning within countries, and can
serve as a guide for CITES listing. The IUCN Red
List Categories and Criteria are the most widely
The IUCN Red List assessment of aspidochirotid sea cucumbers
and its implications
Chantal Conand1,*, Beth Polidoro2, Annie Mercier3,
Ruth Gamboa4, Jean-François Hamel5 and Steve Purcell6
Abstract
This article presents the results from the assessment of sea cucumbers in the order Aspidochirotida for the
International Union for Conservation of Nature (IUCN) Red List of threatened species. The results were
published by IUCN in June 2013. Of 377 species examined, 16 were classified as threatened with extinction
(7 as endangered, 9 as vulnerable) based on standard IUCN methodology. We also summarise findings from
a recent publication about the drivers of extinction risk in these sea cucumbers. The IUCN listing sends a
stern message to resource managers for the conservation of threatened species. The IUCN Red List may also
serve to guide future evaluation by CITES (the Convention on International Trade in Endangered Species of
Wild Fauna and Flora) for listing some of the species on Appendix II or III in order to set conditions on the
trade of those species. We discuss some issues of CITES listing for the Philippines, as a “hotspot” country,
and recommend that sea cucumbers should be re-evaluated for listing on CITES Appendix II and III.
accepted system for classifying extinction risk at
the species level. This article explains the IUCN
Red List categories and the process of conducting
species assessments, as well as presents the species
now listed as threatened and the implications of
this conservation tool.
An IUCN Red List workshop on sea cucumbers
in the order Aspidochirotida (Echinodermata:
Holothuroidea) was held in Cartagena, Colombia
from 17–21 May 2010 (see details in Polidoro et
al. 2011). The workshop brought together regional
and international scientific experts to assess, for the
first time, the conservation status and probability of
extinction for all aspidochirotid species by applying
the assessment methodology of the IUCN Red List
Categories and Criteria (IUCN 2001; 2013).
IUCN Red List methodology
The IUCN Red List Criteria are standardised
quantitative tools to determine each species’
probability of extinction, expressed as a Red List
category. IUCN Red List methodology is the
most widely accepted standard for determining
1 Ecomar Laboratory, La Reunion University and MNHN, Paris, France
2 International Union for the Conservation of Nature (IUCN) Marine Biodiversity Unit, Old Dominion University, Norfolk VA,
23529-0266, USA
3 Department of Ocean Sciences, Memorial University, St. John’s NL, A1C 5S7, Canada
4 College of Science and Mathematics, University of the Philippines Mindanao, Mintal, Davao City 8022, Philippines
5 Society for the Exploration and Valuing of the Environment (SEVE), Portugal Cove-St. Philips NL, A1M 2B7, Canada
6 National Marine Science Centre, Southern Cross University, Coffs Harbour NSW 2450, Australia
* Corresponding author: conand@univ-reunion.fr
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SPC Beche-de-mer Information Bulletin #34 – May 2014
the impact of threats on species populations and
conservation status. The IUCN Red List assessment
process strives to provide the most up-to-date, peer-
reviewed assessment of each species. For this reason,
IUCN Red List assessments for complete taxonomic
clades rely on extensive collaboration with scientific
experts around the world. The process involves
intensive species-specific data collection, review
and updating of data (at least one workshop),
subsequent external reviews and validation by
experts, and several internal Red List consistency
checks before publication on the IUCN Red List of
Threatened Species (www.iucnredlist.org).
There are eight IUCN Red List categories:
Extinct (EX), Extinct in the Wild (EW), Critically
Endangered (CR), Endangered (EN), Vulnerable
(VU), Near Threatened (NT), Least Concern (LC)
and Data Deficient (DD).
A species qualifies for one of the three threatened
categories (CR, EN, or VU) by meeting the threshold
for that category for any one of five criteria (A–E).
These are summarised as follows:
Criterion A — population decline (thresholds:
30% for VU, 50% for EN, and 80% for CR) over
a timeframe of more than 10 years or three
generations.
Criterion B small geographic range size
(extent of occurrence < 20,000 km2 or area of
occupancy < 2,000 km2 to meet the lowest
threshold for VU) combined with continued
decline and habitat fragmentation.
Criterion C species with small population
sizes, estimated to be less than 10,000 mature
individuals, with continued decline.
Criterion D species with less than
1,000 mature individuals, or those with an area
of occupancy < 20 km2, or those that are found
in less than 5 locations as defined by a threat.
Criterion E — species with extensive population
information that allows for population declines
to be appropriately modelled over time.
The category NT is assigned to species that come
close to but do not fully meet all the thresholds or
conditions required for a threatened category under
any criterion, and the category LC is assigned if a
species does not meet or come close to meeting any
of the thresholds required of a threatened category. A
species is listed as DD if there are insufficient data (e.g.
on population declines or geographic range) to apply
the Red List Criteria. This can apply to species that
need taxonomic clarification, or that are only known
from a few specimens or the holotype, as was the case
for the majority of Aspidochirotida in this category. In
some cases, relatively well-known species are listed
as DD when significant threats are known but cannot
be adequately quantified (IUCN 2013).
The order Aspidochirotida contains most of the
sea cucumber species that are under threat from
commercial exploitation. To conduct IUCN Red List
assessments for all 377 known species in this order,
data were compiled on each species’ taxonomy,
distribution, population trends, ecology, life history,
past and existing threats, and conservation actions.
The final comprehensive list of Aspidochirotida
species was based primarily on species listed as
valid on the World Register of Marine Species
(www.marinespecies.org) as of December 2012,
with subsequent refinement by taxonomic experts
(Yves Samyn, pers. comm. 2012; Francisco Solis-
Marin, pers. comm. 2012). Some species were
omitted from the assessment, including a few that
are commercially exploited in multiple countries
(Purcell et al. 2012), because they were known
only by common names and not yet described
taxonomically (e.g. Holothuria spp. type “pentard”).
We also note that there are other commercially
important sea cucumber species (such as those in
the family Cucumariidae, order Dendrochirotida)
that were excluded in this taxonomically based
assessment. The majority of Aspidochirotida
species that met the threshold for a threatened
category were assessed under Criterion A (Purcell
et al. 2014). All maps of geographic ranges and
related analyses (ecoregion, depth) were conducted
in ArcGIS (v. 10.0), as detailed in Purcell et al. 2014.
Red List assessment results
In June 2013, the IUCN Red List for aspidochirotid
holothuroids was published. The complete list
of species along with each species’ individual
assessment account, or report, with all supporting
data and references used for the assessment can be
found by typing “Aspidochirotida” in the search
term at the following site: http://www.iucnredlist.
org/search
The search can be refined by Assessment, and
selecting those Vulnerable and Endangered. The
full assessment information can be found by
clicking on the species names, and each species’
digital distribution map can be found by clicking
on the map icon. Additionally, the complete list
of the 377 species assessed and other supporting
information can be found in the supplemental
online materials in Purcell et al. 2014.
Seven species were classified as “Endangered, or
at a high risk of extinction”, and nine species were
classified as “Vulnerable, or at risk of extinction”
(Table 1).
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SPC Beche-de-mer Information Bulletin #34 – May 2014
Table 1. Species listed as “Endangered, or at a high risk of extinction”, or “Vulnerable, or at risk of extinction”.
Scientific name English common name IUCN status Population trend
Endangered, or at a high risk of extinction
1Apostichopus japonicus Japanese spiky sea cucumber Endangered A2bd ver 3.1 Decreasing
2Holothuria lessoni Golden sandfish Endangered A2bd ver 3.1 Decreasing
3Holothuria nobilis Black teatfish [Indian Ocean] Endangered A2bd ver 3.1 Decreasing
4Holothuria scabra Sandfish Endangered A2bd ver 3.1 Decreasing
5Holothuria whitmaei Black teatfish [Pacific, SE Asia] Endangered A2bd ver 3.1 Decreasing
6Isostichopus fuscus Brown sea cucumber Endangered A2bd ver 3.1 Decreasing
7Thelenota ananas Prickly redfish Endangered A2bd ver 3.1 Decreasing
Vulnerable, or at risk of extinction
1Actinopyga echinites Deepwater redfish Vulnerable A2bd ver 3.1 Decreasing
2Actinopyga mauritiana Surf redfish Vulnerable A2bd ver 3.1 Decreasing
3Actinopyga miliaris Hairy blackfish Vulnerable A2bd ver 3.1 Decreasing
4Apostichopus parvimensis Warty sea cucumber Vulnerable A2bd ver 3.1 Stable
5Bohadschia maculisparsa Vulnerable D2 ver 3.1 Unknown
6Holothuria arenacava Vulnerable D2 ver 3.1 Unknown
7Holothuria fuscogilva White teatfish Vulnerable A2bd ver 3.1 Decreasing
8Holothuria platei Vulnerable D2 ver 3.1 Unknown
9Stichopus herrmanni Curryfish Vulnerable A2bd ver 3.1 Decreasing
Discussion
A recently published paper “The cost of being
valuable: Predictors of extinction risk in marine
invertebrates exploited as luxury seafood” (Purcell
et al. 2014) used the Red List assessment results in
conjunction with other data to assess various factors
that could explain why some species are currently
under threat. That study found that the main driver
of extinction risk was high market value; in other
words, high-value species face the greatest risk of
extinction. Other important drivers were a shallow
depth of occurrence, large geographic range, high
human populations and poor economies in species’
distribution range. That paper contains important
electronic supplementary materials, such as the list
of the 377 species examined, and details on data for
factors used in the analyses.
It emerges that high-value species, particularly those
living in shallow waters, urgently need rigorous
regulatory measures for their exploitation. Because
species-specific bans do not prevent serial depletion
of other species further down the value chain, it
might be advisable to set a shortlist of allowable
species, which excludes threatened species and
those important for ecosystem functions, and to
implement capacity and effort limitations (e.g. short
fishing seasons). These measures will be challenging
to enforce because developing countries, where
average per capita incomes are low, have many
threatened species to manage (i.e. threats to
biodiversity loss are most severe where capacity
is weakest to manage them). International support
(e.g. CITES listings) would be helpful but will
require increasing research and capacity building
in “conservation hotspots”, including countries in
the western Indian Ocean and Coral Triangle, that
exhibit a combination of dense human populations,
coastal poverty and a high number of threatened
sea cucumber species (Purcell et al. 2014).
The Philippines is a conservation hotspot and
offers an example of some of the challenges for
implementing trade agreements such as CITES. The
Philippines has 11 of the 16 threatened aspidochirotid
species, all of which are caught and traded by
small-scale fishers, in open-access, unregulated
fishing grounds. Listing of these 11 species in CITES
Appendix II or III would need to consider the flow-
on effects to fisher livelihoods and would likely be
met with resistance by middlemen and traders. The
Department of Agriculture — Bureau of Fisheries
is presently working to implement minimum legal
size limits for dried beche-de-mer. In addition, the
Philippines has invested in developing technology
to culture sandfish (Holothuria scabra) (Gamboa et al.
2012) and release them in the wild for sea ranching,
and stock restoration is explored (Juinio-Menez et
al. 2013). Those initiatives to improve management
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SPC Beche-de-mer Information Bulletin #34 – May 2014
and recover stocks may help towards conservation
and could be preferable to international trade
restrictions. However, without strong enforcement
and other regulatory measures, the effectiveness
of size limits and restocking in safeguarding
species from extirpation (local extinction) is rather
questionable (Purcell et al. 2013).
While some endangered species are now being
successfully raised in captivity, aquaculture does not
necessarily safeguard extinction in the wild, unless
explicit restoration measures are implemented. This
is exemplified by intensive aquaculture production
and sea ranching of Apostichopus japonicus in
China, which has apparently not resulted in the
recovery of wild populations (Purcell et al. 2014).
The recent IUCN Red List assessment may offer
advocacy for restocking programmes that aim to
recover depleted wild populations because this is
now a global conservation issue for many of the
threatened species. Certain countries may move
to require regulated permits for the collection of
broodstock of threatened species for aquaculture
programmes, and certification that exports are from
cultured stocks.
Regional consultations and/or agreements among
countries are now needed, given the geographical
distribution of commercial species. International
trade regulations have to take these results into
account; species listed as Endangered should
probably be listed on CITES Appendix II and those as
Vulnerable should at least be on Appendix III. In the
past, listing sea cucumber species on CITES has been
encumbered by a deficiency of information tools to
identify species in trade and some uncertainties
regarding taxonomy and biology; these limitations,
however, have been largely addressed in recent
years. As only one species is presently listed in
Appendix III, it is hoped that scientists will be given
the opportunity to collaborate on a new process of
CITES listing to conserve populations and species
at risk.
In conclusion, the Red List classifications of
sea cucumbers serve as a tool for biodiversity
conservation and resource management. Fishing
pressure on sea cucumber populations has been
extraordinarily intense in recent decades across
much of the world (Toral-Granda et al. 2008; Purcell
et al. 2013), placing species and coastal livelihoods at
risk. Preserving both into the future will ultimately
depend on concerted local level regulatory measures
by resource managers and international support.
References
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... Based on several studies, H. scabra is still being exploited throughout its range, even though populations are estimated to have declined by more than 90% in at least 50% of its range and are considered overexploited in at least 30% of its range, although exact declines are difficult to estimate. As a result, H. scabra was listed as an endangered species on the IUCN Red List (Conand et al., 2014b;Hamel et al., 2013). Hamel et al. (2013) mentioned that if fishing pressure was decreased, this species may recover due to its reproductive capacity with several annual spawning events, high fecundity and fast growth rate. ...
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Holothuria scabra is one of the most intensively studied holothuroids, or sea cucumbers (Echinodermata: Holothuroidea), having been discussed in the literature since the early 19th century. The species is important for several reasons: (1) it is widely distributed and historically abundant in several shallow soft-bottom habitats throughout the Indo-Pacific, (2) it has a high commercial value on the Asian markets, where it is mainly sold as a dried product (beche-de-mer) and (3) it is the only tropical holothuroid species that can currently be mass-produced in hatcheries. Over 20 years have elapsed since the last comprehensive review on H. scabra published in 2001. Research on H. scabra has continued to accumulate, fuelled by intense commercial exploitation, and further declines in wild stocks over the entire distribution range. This review compiles data from over 950 publications pertaining to the biology, ecology, physiology, biochemical composition, aquaculture, fishery, processing and trade of H. scabra, presenting the most complete synthesis to date, including scientific papers and material published by local institutions and/or in foreign languages. The main goal of this project was to summarize and critically discuss the abundant literature on this species, making it more readily accessible to all stakeholders aiming to conduct fundamental and applied research on H. scabra, or wishing to develop aquaculture, stock enhancement and management programs across its geographic range.
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Introduction Holothuria tubulosa is one of the most common sea cucumbers in the Mediterranean Sea, generally associated with organically enriched coastal sediments and seagrass beds. As a deposit-feeder, it is responsible for strong bioturbation processes and plays a putative key role in sedimentary carbon cycling and benthic trophodynamics. With the aim of exploring the potential use of holothuroids as a tool for remediating eutrophicated sediments, we investigated the effects of H. tubulosa on sedimentary organic matter quantity, biochemical composition, and nutritional quality. Methods Holothuroids and associated samples of ambient sediments were collected in two sites located in the Central-Western Mediterranean Sea (Sardinia, Italy) and characterized by different trophic status backgrounds: the site of Oristano characterized by sandy-muddy sediments and the presence of mariculture plants (ranked as meso-eutrophic) and the site of Teulada characterized by sandy sediments and Posidonia oceanica meadows (ranked as oligo-mesotrophic). We compared the biochemical composition (proteins, carbohydrates, lipids) of ambient sediment vs sea cucumbers feces and the sedimentary protein content vs protein content in the sediments retrieved in different gut sections (esophagus, mid gut, end gut) of the holothuroid. Results Our results reveal that holothuroids feeding on meso-eutrophic sediments can increase protein (1.5 times) and lipid (1.3 times) content through their defecation, thus making these substrates a more labile food source for other benthic organisms. We report here that H. tubulosa feeding on meso-eutrophic sediment is most likely able to actively select particles rich in labile organic matter with buccal tentacles, as revealed by the protein content in the esophagus that is up to 2-folds higher than that in the source sediment. According to the inverse relationship between assimilation rates and availability of organic substrates and the optimal foraging theory, H. tubulosa feeding on oligo-mesotrophic sediments showed potential assimilation of proteins ca. 25% higher than that of specimens feeding on meso-eutrophic sediments. Discussion Our results reveal that H. tubulosa feeding on meso-eutrophic sediments can profoundly influence the benthic trophic status, specifically modifying the biochemical composition and nutritional quality of organic matter, thus paving the way to its possible use in bioremediation actions of eutrophicated sediments and in Integrated Multi-Trophic Aquaculture systems.
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International Union for Conservation of Nature) IUCN Red List Categories and Criteria Version 3.1 2 nd edition
IUCN (International Union for Conservation of Nature). 2001. IUCN Red List Categories and Criteria Version 3.1 2 nd edition. Gland, Switzerland and Cambridge, IUCN; iv + 32 p.
International Union for Conservation of Nature) 2013. Guidelines for using the IUCN Red List Categories and Criteria. Version 10. Prepared by the Standards and Petitions Subcommittee
IUCN (International Union for Conservation of Nature). 2013. Guidelines for using the IUCN Red List Categories and Criteria. Version 10. Prepared by the Standards and Petitions Subcommittee. http://www.iucnredlist.org/ documents/RedListGuidelines.pdf Accessed March 4, 2013.