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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.
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... Its popularity among other sea cucumbers is due to its thick and rigid body wall and consequent lower weight loss with a wet-to-dry conversion ratio of 18.6% (Ngaluafe and Lee, 2013). High fishing pressure on H. fuscogilva populations led to the status declaration of the species as being vulnerable in the International Union for Conservation of Nature (IUCN) red list of threatened species (Conand et al., 2014). In August 2019, three species of teatfish were added to Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) Appendix II: Holothuria nobilis, H. fuscogilva, and H. whitmaei (Di Simone et al., 2021). ...
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The hatchery production and mariculture of the sea cucumber species Holothuria fuscogilva Cherbonnier, 1980, commonly known as white teatfish, represent a potential remedy for the decreasing population of this extensively exploited species, owing to its considerable nutritional and medicinal value. The Sea Cucumber Research and Development Center at Mindanao State University in Naawan is actively formulating a comprehensive protocol for the large-scale production of H. fuscogilva through hatchery methods. Within hatchery rearing for mass production, selecting an optimal feed type influences the growth and survival rates of H. fuscogilva juveniles. To address this, an experiment employing a complete block randomized design was executed, utilizing four distinct feed types—Navicula sp., tilapia waste + commercial probiotics (CP), Spirulina powder, and commercial feed (mixed feed for Penaeus monodon #1)—each replicated three times. This 90-day laboratory experiment involved 960 individuals of 90-day-old hatchery- reared H. fuscogilva juveniles with an initial weight of 0.11±0.004g. The results revealed that Navicula sp. and Spirulina powder significantly contributed to higher average body weight, average weight gain, growth rate, and specific growth rates compared to commercial feed and tilapia waste + CP. Notably, Navicula sp. demonstrated the highest % survival rate (87.92±3.88%) over the 90 days, surpassing the rates observed for tilapia waste + CP (63.75±7.11%), Spirulina powder (26.67±6.40%), and commercial feed (20.00±4.30%). These findings suggest that the Navicula sp. was the ideal feed for H. fuscogilva juveniles at this stage supporting better survival and growth.
... Its popularity among other sea cucumbers is due to its thick and rigid body wall and consequent lower weight loss with a wet-to-dry conversion ratio of 18.6% (Ngaluafe and Lee, 2013). High fishing pressure on H. fuscogilva populations led to the status declaration of the species as being vulnerable in the International Union for Conservation of Nature (IUCN) red list of threatened species (Conand et al., 2014). In August 2019, three species of teatfish were added to Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) Appendix II: Holothuria nobilis, H. fuscogilva, and H. whitmaei (Di Simone et al., 2021). ...
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The hatchery production and mariculture of the sea cucumber species Holothuria fuscogilva Cherbonnier, 1980, commonly known as white teatfish, represent a potential remedy for the decreasing population of this extensively exploited species, owing to its considerable nutritional and medicinal value. The Sea Cucumber Research and Development Center at Mindanao State University in Naawan is actively formulating a comprehensive protocol for the large-scale production of H. fuscogilva through hatchery methods. Within hatchery rearing for mass production, selecting an optimal feed type influences the growth and survival rates of H. fuscogilva juveniles. To address this, an experiment employing a complete block randomized design was executed, utilizing four distinct feed types-Navicula sp., tilapia waste + commercial probiotics (CP), Spirulina powder, and commercial feed (mixed feed for Penaeus monodon #1)-each replicated three times. This 90-day laboratory experiment involved 960 individuals of 90-day-old hatchery-reared H. fuscogilva juveniles with an initial weight of 0.11±0.004g. The results revealed that Navicula sp. and Spirulina powder significantly contributed to higher average body weight, average weight gain, growth rate, and specific growth rates compared to commercial feed and tilapia waste + CP. Notably, Navicula sp. demonstrated the highest % survival rate (87.92±3.88%) over the 90 days, surpassing the rates observed for tilapia waste + CP (63.75±7.11%), Spirulina powder (26.67±6.40%), and commercial feed (20.00±4.30%). These findings suggest that the Navicula sp. was the ideal feed for H. fuscogilva juveniles at this stage supporting better survival and growth.
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The present work extends the geographical range of Bohadschia atra Massin, Rasolofonirina, Conand, and Samyn (1999) to the Andaman Islands, located in the Bay of Bengal, between 6° and 14°N latitude and 92° and 94°E longitude. The species identification was confirmed using the original description, based on morphological and ossicle structure analysis. The species only previously known distribution record for India was restricted to the Arabian Sea.
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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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Following the FAO International Workshop on the Sustainable Use and Management of Sea Cucumber Fisheries, held in Puerto Ayora, Galapagos Islands, Ecuador, in November 2007 (see Toral-Granda et al. 2008), the global sea cucumber fishery review has been finalized and will be published by the UN Food and Agriculture Organization. The document will be available in November 2008 under the following reference: Toral-Granda V., Lovatelli A. and Vasconcellos M. (eds). 2008. Sea cucumbers. A global review on fishery and trade. FAO Fisheries Technical Paper No. 516. Rome, FAO. 319 p. The executive summary of this document is reproduced below.
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Extinction risk has been linked to biological and anthropogenic variables. Prediction of extinction risk in valuable fauna may not follow mainstream drivers when species are exploited for international markets. We use results from an International Union for Conservation of Nature Red List assessment of extinction risk in all 377 known species of sea cucumber within the order Aspidochirotida, many of which are exploited worldwide as luxury seafood for Asian markets. Extinction risk was primarily driven by high market value, compounded by accessibility and familiarity (well known) in the marketplace. Extinction risk in marine animals often relates closely to body size and small geographical range but our study shows a clear exception. Conservation must not lose sight of common species, especially those of high value. Greater human population density and poorer economies in the geographical ranges of endangered species illustrate that anthropogenic variables can also predict extinction risks in marine animals. Local-level regulatory measures must prevent opportunistic exploitation of high-value species. Trade agreements, for example CITES, may aid conservation but will depend on international technical support to low-income tropical countries. The high proportion of data deficient species also stresses a need for research on the ecology and population demographics of unglamorous invertebrates.
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Worldwide, most sea cucumber fisheries are ineffectively managed, leading to declining stocks and potentially eroding the resilience of fisheries. We analyse trends in catches, fishery status, fishing participation and regulatory measures among 77 sea cucumber fisheries through data from recent fishery reports and fishery managers. Critical gaps in fisheries biology knowledge of even commonly targeted species undermine the expected success of management strategies. Most tropical fisheries are small-scale, older and typified by numerous (>8) species, whereas temperate fisheries are often emerging, mono-specific and industrialized. Fisher participation data indicated about 3 million sea cucumber fishers worldwide. Fisher participation rates were significantly related to the average annual yield. permanova analysis showed that over-exploited and depleted fisheries employed different sets of measures than fisheries with healthier stocks, and a non-metric multidimensional scaling ordination illustrated that a broad set of regulatory measures typified sustainable fisheries. SIMPER and regression tree analyses identified that the dissimilarity was most related to enforcement capacity, number of species harvested, fleet (vessel) controls, limited entry controls and rotational closures. The national Human Development Index was significantly lower in countries with over-exploited and depleted fisheries. Where possible, managers should limit the number of fishers and vessel size and establish short lists of permissible commercial species in multispecies fisheries. Our findings emphasize an imperative to support the enforcement capacity in low-income countries, in which risk of biodiversity loss is exceptionally high. Solutions for greater resilience of sea cucumber stocks must be embedded within those for poverty reduction and alternative livelihood options.
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The potential of sea ranching sandfish (Holothuria scabra) for production and stock restoration was investigated in the Philippines. A total of 14,300 fluorochrome-stained juvenile sandfish (>3 g) were released in 8 batches over a 15-month period in a 5-hectare pilot communal sea ranch. Abundance of sandfish increased from 416 to 5,562 individuals, with a corresponding increase in biomass from 7 to 221 kg ha−1 over the 19-month period. Apparent survival over the study period was estimated at 20–30%. Incidences of in situ spawning were observed in the sea ranch within a year, and estimated densities of reproductively mature sandfish increased from 37 ind ha−1 7 months after initial release to 249 ind ha−1 after 19 months. Average weight at onset of sexual maturity (∼185 g) is estimated to be attained 7–9 months after release. Juveniles without fluorochorome stained ossicles were found during most monitoring periods, indicating presence of wild recruits. A well-managed communal sea ranch has the potential to contribute to fisheries production and stock restoration objectives.
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.