Notice2021-26178
Endangered and Threatened Wildlife and Plants; 12-Month Finding on a Petition To List the Black Teatfish (Holothuria nobilis) as Threatened or Endangered Under the Endangered Species Act
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Published
December 2, 2021
Issuing agencies
Commerce DepartmentNational Oceanic and Atmospheric Administration
Abstract
We, NMFS, have completed a comprehensive status review under the Endangered Species Act (ESA) for the black teatfish (Holothuria nobilis). After reviewing the best scientific and commercial data available, including the H. nobilis Status Review Report, we have determined that listing H. nobilis as a threatened or endangered species under the ESA is not warranted at this time.
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[Federal Register Volume 86, Number 229 (Thursday, December 2, 2021)]
[Notices]
[Pages 68477-68485]
From the Federal Register Online via the Government Publishing Office [<a href="http://www.gpo.gov">www.gpo.gov</a>]
[FR Doc No: 2021-26178]
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DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration
[Docket No. 211122-0242; RTID 0648-XR113]
Endangered and Threatened Wildlife and Plants; 12-Month Finding
on a Petition To List the Black Teatfish (Holothuria nobilis) as
Threatened or Endangered Under the Endangered Species Act
AGENCY: National Marine Fisheries Service (NMFS), National Oceanic and
Atmospheric Administration (NOAA), Department of Commerce.
ACTION: Notice of 12-month finding and availability of status review
document for the black teatfish (Holothuria nobilis).
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SUMMARY: We, NMFS, have completed a comprehensive status review under
the Endangered Species Act (ESA) for the black teatfish (Holothuria
nobilis). After reviewing the best scientific and commercial data
available, including the H. nobilis Status Review Report, we have
determined that listing H. nobilis as a threatened or endangered
species under the ESA is not warranted at this time.
DATES: This finding was made on December 2, 2021.
ADDRESSES: The H. nobilis Status Review Report associated with this
determination, its references, and the petition can be accessed
electronically online at: <a href="https://www.fisheries.noaa.gov/species/black-teatfish#conservation-management">https://www.fisheries.noaa.gov/species/black-teatfish#conservation-management</a>.
FOR FURTHER INFORMATION CONTACT: Celeste Stout, NMFS Office of
Protected Resources, 301-427-8436.
SUPPLEMENTARY INFORMATION:
Background
On May 14, 2020, we received a petition from the Center for
Biological Diversity to list black teatfish (H. nobilis) as a
threatened or endangered species under the ESA. The petition asserted
that H. nobilis is threatened by four of the five ESA section 4(a)(1)
factors: (1) The present or threatened destruction, modification, or
curtailment of its habitat or range; (2) overutilization for commercial
purposes; (3) inadequacy of existing regulatory mechanisms; and (4)
other natural or manmade factors.
On August 10, 2020, NMFS published a 90-day finding for H. nobilis
with our determination that the petition presented substantial
scientific and commercial information indicating that
[[Page 68478]]
the petitioned action may be warranted (85 FR 48144). We also announced
the initiation of a status review of the species, as required by
section 4(b)(3)(a) of the ESA, and requested information to inform the
agency's decision on whether this species warrants listing as
endangered or threatened under the ESA. We received information from
the public in response to the 90-day finding and incorporated the
information into both the Status Review Report (NMFS 2021) and this 12-
month finding.
Listing Determinations Under the ESA
We are responsible for determining whether H. nobilis is threatened
or endangered under the ESA (16 U.S.C. 1531 et seq.). To be considered
for listing under the ESA, a group of organisms must constitute a
``species,'' which is defined in section 3 of the ESA to include any
subspecies of fish or wildlife or plants, and any distinct population
segment (DPS) of any species of vertebrate fish or wildlife which
interbreeds when mature (16 U.S.C. 1532(16)). Because H. nobilis is an
invertebrate species, the ESA does not permit listing its populations
as DPSs.
Section 3 of the ESA defines an endangered species as any species
which is in danger of extinction throughout all or a significant
portion of its range and a threatened species as one which is likely to
become an endangered species within the foreseeable future throughout
all or a significant portion of its range 16 U.S.C. 1532(6), 16 U.S.C.
1532(20). Thus, in the context of the ESA, we interpret an ``endangered
species'' to be one that is presently in danger of extinction. A
``threatened species,'' on the other hand, is not presently in danger
of extinction, but is likely to become so in the foreseeable future
(that is, at a later time). In other words, the primary statutory
difference between a threatened and endangered species is the timing of
when a species is in danger of extinction, either presently
(endangered) or not presently but in the foreseeable future
(threatened).
When we consider whether a species qualifies as threatened under
the ESA, we must consider the meaning of the term ``foreseeable
future.'' Regulations at 50 CFR 424.11(d) state that the foreseeable
future extends only so far into the future as we can reasonably
determine that both the future threats and the species' responses to
those threats are likely. What constitutes the foreseeable future for a
particular species depends on case-specific factors such as the the
species' life-history characteristics, threat-projection timeframes,
and environmental variability. That is, the foreseeability of a
species' future status is case specific and depends upon both the
foreseeability of threats to the species and foreseeability of the
species' response to those threats.
The statute requires us to determine whether any species is
endangered or threatened throughout all or a significant portion of its
range as a result of any one or a combination of any of the following
five factors: (A) The present or threatened destruction, modification,
or curtailment of its habitat or range; (B) overutilization for
commercial, recreational, scientific, or educational purposes; (C)
disease or predation; (D) the inadequacy of existing regulatory
mechanisms; or (E) other natural or manmade factors affecting its
continued existence (16 U.S.C. 1533(a)(1)). We are also required to
make listing determinations based solely on the best scientific and
commercial data available, after conducting a review of the species'
status and after taking into account efforts, if any, being made by any
state or foreign nation (or subdivision thereof) to protect the species
(16 U.S.C. 1533(b)(1)(A)).
To determine whether H. nobilis warrants listing under the ESA, we
completed a Status Review Report (NMFS 2021), which summarizes the
taxonomy, distribution, abundance, life history, and biology of the
species. The Status Review Report (NMFS 2021) also identifies threats
or stressors affecting the status of the species, and provides a
description of fisheries and fisheries management. NMFS then assessed
the threats affecting H. nobilis as well as demographic risk factors
(abundance and trends, population growth rate or productivity, spatial
structure and connectivity, and genetic diversity) as part of an
extinction risk analysis (ERA). The results of the ERA from the Status
Review Report (NMFS 2021) are discussed below. The Status Review Report
incorporates information received in response to our request for
information (85 FR 48144, August 10, 2020) and comments from three
independent peer reviewers. Information from the Status Review Report
is summarized below in the Biological Review section.
Biological Review
This section provides a summary of key biological information
presented in the Status Review Report (NMFS 2021).
Species Description
Sea cucumbers are characterized by a suboval body arched dorsaly
and flattened ventrally, a thick and rigid tegument, a large number of
ventral podia arranged tightly and without order, small dorsal
papillae, and anal teeth (Purcell et al. 2012). The mouth, surrounded
by tentacles, is ventral (Purcell et al. 2012). The main characteristic
that distinguishes teatfish from other sea cucumber species is the
presence of lateral protuberances (``teat-like'') on their body
tegument (outer body covering) visible in their live and processed
forms (Purcell et al. 2012; Conand pers. comm. 2017 in CITES 2019).
H. nobilis is black dorsally with white blotches and spots on the
sides of the animal and around the lateral protrusions (`teats'). H.
nobilis has between 6 to 10 characteristic large lateral protrusions at
the ventral margins. The average length of H. nobilis is about 35 cm,
but has been observed at up to 60 cm. The presence of dorsal podia are
sparse and small, while the ventral podia are numerous, short and
greyish. The tegument is usually covered by fine sand. The mouth is
ventral, with 20 stout tentacles and the anus is surrounded by five
small calcareous teeth.
Range, Distribution, and Habitat Use
H. nobilis occurs in tropical coral reef flats and outer reef
slopes at depths between 0 and 40 meters, with a preference for hard
substrates (Lawrence et al. 2004; Idreesbabu and Sureshkumar 2017;
Eriksson et al. 2012; Conand et al. 2013; CITES 2019). While H. nobilis
has occasionally been observed in seagrass (Purcell et al. 2012),
seagrass is not considered the desired habitat of the species. Lawrence
et al. (2004) state that while seagrass beds may be important to most
of the main commercial species of sea cucumber, H. nobilis is one of
the exceptions as it had only been found on coral substrate. Further,
H. nobilis is considered to be strongly associated with a single
habitat variable (i.e. hard substrate; Eriksson et al. 2012). Thus, the
primary habitat for H. nobilis is widely considered to be coral reefs
(flats/slopes; Conand 2008). H. nobilis is commonly seen covered by
sand, though this species does not bury itself (Conand 2008). H.
nobilis is distributed throughout the Indian Ocean, including along the
east coast of Africa (Egypt, Sudan, Somalia, Kenya, Eritrea, Djibouti,
Tanzania, Mozambique, Zanzibar, and South Africa); the Red and Arabian
Seas (Israel, Jordan, Saudi Arabia, Oman, Yemen); and the coastal
waters of Madagascar, Mayotte, Mauritius, La Reunion, Seychelles,
Comoros, Chagos, Sri Lanka, the
[[Page 68479]]
Maldives, and the west coast of India (See Figure 5 in NMFS 2021; CITES
2019; Conand et al. 2013; Uthicke et al. 2004). The species does not
occur in the waters of the United States or its overseas territories.
Diet and Feeding
H. nobilis like other sea cucumbers of the order Holothuriida are
deposit and detritus feeders. They digest organic matter in the
sediment such as bacteria, cyanobacteria, decaying plant matter,
copepods, diatoms, foraminiferans, and fungi. Using their retractile
tentacles, they ingest the top few millimeters of sediment and excrete
less organic rich sediment (Anderson et al. 2011; Purcell et al. 2016;
Webster & Hart 2018).
Reproductive Biology
Teatfish are gonochoristic (i.e. separate sex) broadcast spawners,
meaning males and females release their gametes into the water column
and fertilization occurs externally (Conand 1981; Conand 1986; Toral-
Granda 2006). H. nobilis do not exhibit sexual dimorphism, and sex of
individual animals must be determined through microscopic examination
of the gonads.
Teatfish have slow growth rates, maturing at about 3-7 years, and
are thought to live for several decades (Conand et al. 2013, FAO 2019).
Conand et al. (2013) reported that H. nobilis mature at around 4 years
of age. Reproductive fitness is positively correlated with body size,
with larger individuals having larger gonads that produce more gametes,
thus exhibiting higher fecundity (CITES 2019). As adults, they are non-
migratory and relatively sedentary (FAO 2019).
Environmental cues (e.g., tidal conditions, lunar phases,
temperature fluctuations) and chemical cues trigger the release of
gametes (Purcell et al. 2010). H. nobilis is believed to reproduce
annually during the cold season (Purcell, Samyn & Conand 2012; Conand
et al. 2013; CITES 2019). Successful fertilization depends upon
sufficient population density and proximity of adults (Purcell et al.
2010; Purcell et al. 2011; CITES 2019; FAO 2019). Minimum population
densities for successful reproduction have yet to be determined
(Purcell et al. 2011).
The oocytes of most sea cucumber species, which include teatfish,
are small (< 200 [mu]m in diameter) and are neutrally buoyant in the
water column (Purcell et al. 2010). Fertilized H. nobilis eggs quickly
develop into free[hyphen]swimming larvae--sometimes within a day
(Purcell et al. 2010). These larvae spend 50-90 days in planktonic
stage feeding on algae and may be widely dispersed by ocean currents
(Conand 2009; Purcell et al. 2010; CITES 2019). One breeding trial
found that the planktonic period of H. nobilis ranged from 44-51 days
(Minami 2011). After metamorphosis, sea cucumbers settle on the
seafloor (Conand 2009; Purcell et al. 2010).
Population Structure
H. nobilis was once considered to be H. fuscogilva, another species
of teatfish, but was separated in 1980 (Cherbonnier 1980). In 2004, H.
nobilis was once again separated. H. nobilis now only occurs in the
indian Ocean, while H. whitmaei, occurs in the Pacific Ocean (Uthicke
et al. 2004). The two black teatfish (H. whitmaei, with distribution in
the Pacific Ocean, and H. nobilis, with distribution in the Indian
Ocean) appear to be allopatric with a genetic distance of 9.2 percent,
implying a divergence during the Pliocene of approximately 1.8-4.6
million years ago (Uthicke et al. 2004). Further molecular analyses
support the distinction between H. nobilis and H. fuscogilva as
different species (Ahmed et al. 2016). Apart from these genetic data
indicating separation of H. nobilis and H. whitmaei (Uthicke et al.
2004), there is very limited additional species-specific information
regarding the population structure or genetics of H. nobilis
populations.
Abundance and Trends
Few standardized datasets documenting changes in teatfish species
densities exist for any range countries. This is due mostly to a lack
of detailed historical data on early harvests (Friedman et al. 2011).
Sea cucumber fisheries are largely made up of artisanal fishers living
in remote locations far removed from the enforcement of centralized
fisheries management agencies and therefore have generally not been
monitored long-term. Additionally, few countries record catches or
exports by species, making it difficult to determine the utilization of
a single species. Despite sea cucumbers high commercial value, there
have been no obvious extirpations of teatfish (type of sea cucumber)
species at the national scale. However, declines in densities of
teatfish (individuals per hectare) are reported from time series and
snap-shot studies, and depletion of stocks have been observed (Kinch et
al. 2008; Hasan and El-Rady, 2012; Friedman et al. 2011; Lane and
Limbong, 2013; Ducarme 2016; FAO 2019). It is also important to note
that similar to other teatfish species, H. nobilis is thought to be
naturally rare when compared to other species of sea cucumber (Purcell,
pers. comm. 2019 in CITES 2019; CITES 2019; Conand et al. 2013; Uthicke
et al. 2004).
While data on abundance and population trends for teatfish are
lacking, they are even more sparse for H. nobilis (Anderson et al.
2011). The mean density of H. nobilis in areas where the species has
been observed/surveyed (e.g., Chagos, Egypt, Eritrea, Madagascar,
Mayotte, Saudi Arabia, Seychelles, Sri Lanka, and Zanzibar) ranges from
approximately 0.12 to 10 individuals per hectare (CITES 2019). It is
thought that H. nobilis once occurred at much greater densities (Conand
2018), with anecdotal reports from sea cucumber collectors indicating
that sea cucumbers, in general, were historically larger in size and
more abundant (Mmbaga 2013). Throughout the range of H. nobilis, this
species is considered less abundant relative to previous surveys or
anecdotal data or its status is uncertain or unknown based on a lack of
data. In fact, in 18 of the 25 countries where H. nobilis is reported
to occur, the abundance of the species and trends in abundance is very
limited or unknown. The information available for the other seven range
countries (i.e, Chagos, Egypt, Madagascar, Mayotte, Saudi Arabia,
Seychelles, and Tanzania) indicates that there are possible declines in
abundance with one exception--the Seychelles, where it is reported to
be stable (Conand et al. 2013, FAO 2019, CITES 2019). Overall, while
some quantitative data are available, the abundance and density trends
of H. nobilis across its range are poorly understood. Abundance
information by country is summarized in Table 1 of NMFS 2021.
Extinction Risk Analysis
NMFS relied on the best information available to conduct an
extinction risk analysis through evaluation of four demographic
viability factors and five threats-based listing factors. In
determining the extinction risk of a species, it is important to
consider both the demographic risks facing the species as well as
current and potential threats that may affect the species' status. To
this end, a demographic analysis was conducted for H. nobilis and
considered alongside the information presented on threats as detailed
in the Status Review Report (NMFS 2021).
A demographic risk analysis is an assessment of the manifestation
of past threats that have contributed to the species' current status
and informs the consideration of the biological response of the species
to present and future threats. This analysis evaluated the population
viability characteristics and
[[Page 68480]]
trends available for H. nobilis, such as abundance, growth rate/
productivity, spatial structure, connectivity, and diversity to
determine the potential risks these demographic factors pose to the
species. The information from this demographic risk analysis in
conjunction with the available information on the section 4(a)(1)
factors was then synthesized to determine an overall risk of extinction
for H. nobilis.
The appropriate time horizon for evaluating whether a species is
more likely than not to be at a high level of risk in the ``foreseeable
future'' depends on various case-and species-specific factors. For
example, the time horizon may reflect certain life history
characteristics (e.g., long generational time or late age-at-maturity)
and may also reflect the time frame or rate over which identified
threats are likely to impact the biological status of the species
(e.g., the rate of disease spread). The appropriate time horizon
coincides with the period of time over which reliable projections can
be made as to the specific threats facing the species as well as the
species' response, but it is not limited to the period that status can
be quantitatively modeled or predicted within predetermined limits of
statistical confidence. Reliable projections may be qualitative in
nature.
The ``foreseeable future'' for this extinction risk analysis was
considered to extend out several decades (>30 years). Because of the
species' life history traits, with longevity estimated to be several
decades, age of sexual maturity ranging from three to seven years,
density-dependent reproduction and potentially low rates of
recruitment, it would likely take more than a few decades for any
recent management actions to be realized and reflected in population
abundance. Similarly, the impact of present threats to the species
could be realized in the form of noticeable population declines within
this timeframe, as demonstrated in the available survey and fisheries
data (see Populations and Abundance section in NMFS 2021). As the main
potential operative threats to the species are overutilization and the
inadequacy of existing regulatory mechanisms, this timeframe would
allow for reliable predictions regarding the impact of current levels
of fishery-related mortality on the biological status of the species.
Additionally, this time frame allows for consideration of the impacts
on habitat from climate change while the significance of these effects
are still uncertain.
The ability to determine and assess risk factors to a marine
species is often limited when quantitative estimates of abundance and
life history information are lacking. Therefore, in assessing threats
and subsequent extinction risk of a data-limited species such as H.
nobilis, we include both qualitative and quantitative information. In
assessing extinction risk to H. nobilis, we considered the demographic
viability factors developed by McElhany et al. (2000) and the risk
matrix approach developed by Wainwright and Kope (1999) to organize and
summarize extinction risk considerations. In this approach, the
collective condition of individual populations is considered at the
species level according to four demographic viability factors:
Abundance, productivity, spatial structure/connectivity, and diversity.
These viability factors reflect concepts that are well-founded in
conservation biology and that individually and collectively provide
strong indicators of extinction risk.
Using these concepts, we evaluated extinction risk by assigning a
risk level to each of the four demographic viability factors and five
threats-based listing factors. The levels are defined as follows:
<bullet> Low risk: Based on the best available information, it is
unlikely this threat is causing negative impacts to the species at the
population level throughout its range, such that it is not likely to be
affecting extinction risk for the species:
<bullet> Moderate risk: Based on the best available information,
this threat is likely causing negative impacts to the species at the
population level in at least some portion of its range, such that it
may be affecting extinction risk for the species; and
<bullet> High risk: Based on the best available information, this
threat is likely causing negative impacts to the species at the
population level throughout its range, such that it is likely affecting
extinction risk for the species.
Aditionally, we provided a confidence rating to the impact of each
threat as well as the demographic factors based on the available
information. The confidence rating scores were adapted from Lack et al.
(2014) and are defined as follows:
<bullet> 0 (no confidence) = No information;
<bullet> 1 (low confidence) = Very limited information;
<bullet> 2 (medium confidence) = Some reliable information
available, but reasonable inference and extrapolation required; and
<bullet> 3 (high confidence) = Reliable information with little to
no extrapolation or inference required.
We also considered the potential interactions among demographic and
listing factors. Finally, we examined the levels assigned to each
demographic and listing factor along with the uncertainty rating to
determine the overall risk of extinction (see Extinction Risk
Determination below).
Demographic Risk Analysis
Abundance
As discussed in the Abundance and Trends section of the Status
Review Report, across the range of H. nobilis, the species is either
considered less abundant, or its status is unknown based on a lack of
data, with the exception of the Seychelles (see Table 1 in NMFS 2021).
In fact, in 18 of the 25 countries where H. nobilis is reported to
occur, the abundance of the species and trends in abundance are unknown
due to a lack of data. Similar to other teatfish species, H. nobilis is
thought to be naturally rare when compared to other species of sea
cucumber (Purcell, pers. comm. 2019 in CITES 2019; CITES 2019; Conand
et al. 2013; Uthicke et al. 2004).
H. nobilis has not been reported to be extirpated from any range
countries but has been observed to no longer occur at several survey
locations within some some countries across its range, including Geyser
Bank in Mayotte and Eel Garden in Egypt (see Table 1 in NMFS 2021;
CITES 2019; Conand et al. 2013; Uthicke et al. 2004). Throughout the
species's range, the historical abundance of H. nobilis is uncertain,
but the abundance of other sea cucumber species have been reported to
be declineing (Kinch et al. 2008; Hasan and El-Rady, 2012; Friedman et
al. 2011; Lane and Limbong, 2013; Ducarme 2016; FAO 2019). The
available data indicate population declines or possible population
declines of H. nobilis at survey locations in Chagos, Egypt,
Madagascar, Mayotte, Saudi Arabia, and Tanzania. In Chagos at Salomon
atoll, there was a decrease in density from 83 ind. ha<SUP>-1</SUP> to
10 ind. ha<SUP>-1</SUP> from 2002-2006 (Price et al. 2010). In Egypt,
at Wadi Quny and Eel Garden in the Gulf of Aqaba the species was
observed at densities of 0.7 ind. ha<SUP>-1</SUP> and 1.3 ind.
ha<SUP>-1</SUP> respectively in 2002, but were not observed at these
locations in 2006 (Hasan & El-Rady, 2012). However, confirmed reports
of the species were made off Pharoan Island in April 2015 (Hasan &
Johnson 2019) and H. nobilis has been reported to be commonly seen by
divers as recently as 2019 in Egypt's waters (FAO 2019). For
Madagascar, there are anecdotal reports that H. nobilis is assumed to
be depleted as
[[Page 68481]]
very few specimens have been seen in the past several years (Conand
pers. comm. 2010 in Conand et al. 2013). In Mayotte, the species was
reported to be observed less frequently in 2016 than in 2005, 2012, and
2015, however, we do not have reported density numbers (Mulochau 2018;
FAO 2019). Off the coast of Saudi Arabia, H. nobilis was not documented
in 2004's harvested species but had been present in the harvest record
from 1999-2003. However, in 2006 H. nobilis was observed at 3 of 18
surveyed sites along the coast of Saudi Arabia (Hasan 2008; Hasan
2009). For Tanzania, there are anecdotal reports that H. nobilis once
previously dominated the sea cucumber fishery, but now it is reported
to comprise a very small percentage of the total catch (Conand &
Muthiga 2007). The abundance of H. nobilis in the Seychelles is
reported to be stable (Conand et al. 2013; FAO 2019; CITES 2019).
Adult density is critical to the species' persistence because the
species needs a sufficient density to successfully reproduce (Conand &
Muthiga 2007; Purcell et al. 2010; Purcell et al. 2011). However, due
to the limited species-specific information on H. nobilis throughout
its range it is not possible to determine whether current densities are
adequate to allow for successful reproduction. Research is required to
determine minimum population densities for positive rates of population
growth (Friedman et al. 2011). Overall, while some quantitative data
are available, the abundance and density trends of H. nobilis across
their range are poorly understood.
Productivity
Teatfish generally exhibit low natural mortality rates, low to
moderate population growth rates, and variable success of larval
survival and recruitment, resulting in generally low productivity
(CITES 2019; FAO 2019). While larger individuals may be considered
highly fecund, teatfish experience high levels of larval mortality
(Uthicke, 2004; FAO 2019). Additionally, successful reproduction is
highly dependent on adult density (Conand & Muthiga 2007; Purcell et
al. 2010; Purcell et al. 2011). How productivity may affect the
extinction risk of H. nobilis specifically is challenging to determine
given the lack of species-specific information. As stated ealier, there
have been documented abundance declines (see Table 1 in MNFS 2021) in
Chagos (Saloman Atoll), Mayotte, Egypt (Wadi Quny and Eel Gardens in
the Gulf of Aqaba); however, divers have reported commonly seeing H.
nobilis in Egypt's waters as recently as 2019 (FAO 2019). The remaining
22 range countries do not have species-specific abundance or population
growth data. While population declines due to overharvest could
negatively affect the species's reproduction and survival, we do not
have the data to determine if this is currently affecting H. nobilis,
as minimum population densities for successful reproduction have yet to
be determined (Purcell et al. 2011).
Spatial Structure/Connectivity
H. nobilis has a relatively large range, occurring throughout the
Indian Ocean, including along the east coast of Africa, the Red and
Arabian Seas, the coastal waters of Madagascar and the west coast of
India (CITES 2019; Conand et al. 2013; Uthicke et al. 2004). While
there have been reports of population declines, no widespread
extirpations or a reduction of range have been reported. Additionally,
no information is available on the population structure of H. nobilis
within its range or the connectivity of populations throughout its
range. We considered using other species of teatfish as a reference for
connectivity. Skillings et al. 2014, discussed the connectivity of H.
whitmaei and H. atra in the Hawaiian Islands and showed that species
with similar range sizes do not predict relative dispersal ability.
Both species appeared to share similar life history traits, similar
minimum larval duration, occupy the same habitats, are both wide
ranging, and are closely related, yet they did not have similar levels
of population structuring based on analyses of their genetic data.
Thus, differences in population structure may stem from subtle,
species-specific differences in habitat usage, population size, or life
history that also have large impacts on genetic structure (Skillings et
al 2014). Given these species-dependent results, it would be
inappropriate to use another species of teatfish as a proxy for
determining if current spatial structure and connectivity of
populations are contributing to the extinction risk of H. nobilis.
Diversity
We could not find any information regarding H. nobilis specific
genetic diversity. Without any genetic analyses to determine diversity
or effective population size, we are unable to conclude whether low
genetic diversity is a threat contributing to the species' risk of
extinction.
Summary of Demographic Risk Analysis
In the Status Review Report the risk rating to the species for
Abundance, Productivity, and Spatial Distribution/Spatial Connectivity
was unknown with a confidence rating of 1 and for Genetic Diversity the
rated risk to the species was also unknown with a confidence rating of
0. Thus, we conclude that, while H. nobilis will likly experience
future reductions in abundance due to overutilization for international
trade (discussed in the Analysis of Section 4(a)(1) Factors section),
we are unable to reliably predict the biological or behavioral response
of H. nobilis to this change, and we therefore do not have reliable
information showing that the magnitude of this change could be
sufficient to put the species in danger of extinction now or in the
foreseeable future.
Analysis of Section 4(a)(1) Factors
The Present or Threatened Destruction, Modification, or Curtailment of
Its Habitat or Range
As described in the Status Review Report (NMFS 2021), the available
data do not provide us with an understanding of H. nobilis's habitat
usage, thus, it is difficult to identify any specific present or future
threats that may affect the features of the habitat on which the
species relies. As an alternative, we focus our discussion in the
Status Review Report on threats to coral reef habitat as a whole and
while there is clear evidence that coral reefs (i.e., H. nobilis
habitat) will undergo substantial changes due to impacts from ocean
warming, acidification, and a variety of other threats, it is unclear
whether and to what degree the changes in coral reef composition and
ecological function will affect the extinction risk of this sea
cucumber species throughout its range. While the habitat complexity
provided by the morphological structure of many corals may change due
to selective elimination of certain coral species, there is no
information to suggest which features of the coral reef or species of
coral H. nobilis may be dependent on. Consequently, it is difficult to
predict how the loss of coral reef habitat or changes in coral reef
composition will directly affect extinction risk for H. nobilis. We
recognize that the changes in coral reef habitat predicted over the
next several decades will likely negatively affect sea cucumber
populations; but whether these impacts will significantly increase the
extinction risk of H. nobilis is unclear. Thus, the rated risk to the
species assigned in the Status Review
[[Page 68482]]
Report was unknown with a confidence rating of 1.
Overutilization for Commercial, Recreational, Scientific, or
Educational Purposes
The harvest of H. nobilis for the purpose of supplying Asian
markets with b[ecirc]che-de-mer (i.e., the processed form of sea
cucumbers, either boiled, dried, or smoked), is considered to be the
greatest threat to the species. This harvest has resulted in declines
in local population abundance of sea cucumbers since the early 1990s.
Many of the harvested populations of sea cucumbers, including across
the range of H. nobilis, are considered either to be fully exploited,
overexploited, or depleted (See Figure 8 in NMFS 2021; Purcell et al.
2011). Teatfish species, including H. nobilis, are largely exploited in
small-scale and artisanal fisheries throughout their range. Harvest at
these scales has proven difficult to manage, with booms in fishing
typically followed by closures or moratoriums on fishing once stocks
have been depleted. Overall, there is little international or regional
coordination in management of these fisheries (FAO 2019).
We assume that demand for `high value' sea cucumber species,
including H. nobilis will continue. The extent to which harvest is
impacting H. nobilis populations in the Western Indian Ocean is largely
unknown, although there are some indications that overharvest may be
impacting populations in Chagos, Egypt, Madagascar, Mayotte, Saudi
Arabia, and Tanzania as there have been documented declines in
abundance.
Additionally, there is a lack of recent fisheries-dependent data as
many of the countries have banned sea cucumber fishing, including
Comoros, Egypt, India, Mauritius, Mayotte, Saudi Arabia, Tanzania, and
Yemen. However, despite these bans, there is evidence of continued
fishing pressure on sea cucumbers through illegal, unregulated, and
unreported (IUU) fishing. IUU fishing is common in the range of H.
nobilis (depicted in Figure 10 in NMFS 2021). Evidence of illegal
fishing has specifically been documented in Saudi Arabia, Mayotte,
Yemen, Egypt, Mauritius, and Tanzania.
Finally, overall and country specific trade data for H. nobilis are
unknown. The trade value chains and fishery-to-market tracing do not
provide species-level data. An estimated 10,000 tons of b[ecirc]che-de-
mer are traded internationally each year, corresponding to about 200
million individuals harvested (Purcell et al. 2016). B[ecirc]che-de-
mer, including H. nobilis, are sold primarily to Asian markets in the
Hong Kong Special Administrative Region (SAR), Singapore, Taiwan,
People's Republic of China, Korea, and Malaysia (CITES 2019; Purcell et
al. 2012). H. nobilis is sold for 20 U.S. Dollars (USD) to 80 USD/kg
dry weight, depending on size and condition; prices in Hong Kong retail
markets range from 106 USD to 139 USD/kg dried (Purcell et al. 2012).
However, this product may now have a higher retail price. Purcell et
al. 2018 report that demand, and hence prices of most b[ecirc]che-de-
mer species appear to have steadily increased since 2011; however, this
study did not cover the value of H. nobilis. Being of high value,
teatfish species are preferentially targeted by fishers and exporters.
While H. nobilis may be following similar trends to other `high-value'
species, the lack of species-specific data makes it difficult to know
to what extent.
Based on the above information, the rated risk to the species
assigned in the Status Review Report was moderate with a confidence
rating of 2.
Disease and Predation
The extent to which disease and parasites result in sea cucumber
mortality in the wild is largely unknown. The impact of predation as a
threat on H. nobilis also remains unknown. Thus, the rated risk to the
species assigned in the Status Review Report was unknown with a
confidence rating of 0.
Inadequacy of Existing Regulatory Mechanisms
The establishment of management strategies for H. nobilis has been
and still is hindered by a lack of basic biological and ecological
information as well as limited information on existing and historical
sea cucumber fisheries (Bruckner 2006). The regulatory measures most
common in sea cucumber fisheries for the Indo-Pacific are minimum legal
size limits, gear restrictions (bans on the use of scuba), requirements
for exporters to submit logbooks, and no-take reserves (FAO 2013;
Purcell et al. 2011). There are sea cucumber fishing bans in place in
Yemen, Egypt, Mauritius, Saudi Arabia, Tanzania, and Mayotte (Hasan
2009; Eriksson et al. 2012; FAO 2013). Madagascar's sea cucumber
fisheries regulate the minimum legal size of capture to 11 cm body
length for all sea cucumbers. They also prohibit the use of scuba for
the collection of sea cucumbers (FAO 2013). India has banned the export
of all wild taken specimens of species listed under CITES Appendix I,
II, and III and heavy fines and imprisonment can be imposed (FAO 2013).
The Seychelles has a licensing program that requires an annual sea
cucumber fishing and processing license be purchased. Since 2001, a
maximum of 25 licenses have been distributed each year. Additionally,
fishers' logbooks are required to be submitted regularly. Non-
compliance can result in non-renewal of their fishing license
(Aumeeruddy and Conand 2008). The assessment of individual species and
fishing effort are necessary to determine whether these existing
regulations are likely to be effective at maintaining the
sustainability of the resources. To date, however, the harvest of H.
nobilis and its impact on the population has not been assessed.
Another regulatory mechanism that will affect H. nobilis is the
Convention on International Trade in Endangered Species of Wild Fauna
and Flora (CITES)--an international agreement between governments
established with the aim of ensuring that international trade in
specimens of wild animals and plants does not threaten their survival.
H. nobilis is newly listed under Appendix II of CITES. In total three
species of teatfish were listed under Appendix II of CITES in 2019
(with an effective date of August 2020); H. whitmaei, H. fuscogilva,
and H. nobilis. The Food and Agriculture Organization of the United
Nations (FAO) establishes an expert Panel in advance of each CITES
Conference of the Parties (CoP) to review marine species proposals.
This Expert Panel is tasked with assessing proposals from a scientific
perspective and in accordance with CITES biological listing criteria
(FAO 2008-2021). The assessment of this proposal concluded that H.
whitmaei met the CITES Appendix II listing criteria, while H.
fuscogilva did not meet the listing criteria, and a determination could
not be made for H. nobilis due to insufficient data. However, all three
species were listed under Appendix II of CITES under a ``look-alike''
provision.
Appendix II includes species that are not necessarily threatened
with extinction, but for which trade must be controlled in order to
avoid utilization incompatible with their survival. International trade
of Appendix II species is permitted when export permits are granted
from the country of origin. In order to issue an export permit, the
exporting country must find that the animals were legally obtained and
their export will not be detrimental to the survival of the species in
the wild (referred to as a ``non-detriment finding'').
The extent to which existing regulatory mechanisms are inadequate
[[Page 68483]]
to protect H. nobilis populations from the main threat identified
(i.e., international trade) is difficult to evaluate. We concluded that
while there are some regulatory mechanisms in place with the intent to
control harvest, the enforcement of these regulations is insufficient
and may be negatively affecting population abundance. However, because
international trade is the main threat to the species (i.e.,
overutilization for commercial purposes), the new CITES listings may
provide some safeguards against future depletion of populations.
While local sea cucumber regulations (e.g., moratoriums, fishing
bans, limited entry into the fishery, size restrictions, and gear
restrictions) throughout the range of H. nobilis may be adequate to
protect the species from legal overutilization, the enforcement of
these regulations is inadequate as evidenced by the continued IUU
fishing that occurs in many parts of the species's range and may be
contributing to population declines. Thus, we concluded that inadequacy
of regulatory mechanisms presents a moderate extinction risk with a
confidence rating of 2.
Other Natural or Manmade Factors Affecting Its Continued Existence
We considered factors including bycatch and effects of climate
change on H. nobilis. However, as the primary habitat of H. nobilis is
coral reefs, bycatch by trawlers that mainly trawl sea grass habits are
not likely to have an effect on the extinction risk of H. nobilis.
Additionally, the available literature does not indicate that H.
nobilis has been observed as bycatch in these fisheries (Bruckner
2006). While climate change is a concern, there is a lack of data on
how the effects of climate change (warming waters, acidification, and
sea level rise) may affect H. nobilis. At this time, we were unable to
find any information on other natural or manmade factors that may be
affecting the continued existence of H. nobilis. Thus, the rated risk
to the species assigned in the Status Review Report was unknown with a
confidence rating of 0.
Extinction Risk Determination
Guided by the results of the demographic risk and section 4(a)(1)
factor analyses above, we analyzed the overall risk of extinction of H.
nobilis throughout its range. In this process, we considered the best
available scientific and commercial information regarding H. nobilis
across its range, including associated uncertainties, and analyzed the
collective condition of its populations to assess the species's overall
extinction risk.
Despite much uncertainty due to limited information, it is likely
that H. nobilis will continue to experience declining trends in its
abundance and productivity in the foreseeable future, specifically due
to continued overutilization and the lack of enforcement of existing
regulatory mechanisms. Whether current protective efforts for H.
nobilis (i.e., the recent CITES listing and fishing bans described
above) are or will be effective is uncertain, as described above.
Information on the abundance and distribution of teatfish stocks in
general does not indicate any wide-spread extirpations or a reduction
of range, although declines in densities of teatfish have been reported
from time series and snap-shot studies (Kinch et al. 2008; Hasan and
El-Rady, 2012; Friedman et al. 2011; Lane and Limbong, 2013; Ducarme
2016; FAO 2019). For H. nobilis specifically, declines were recorded in
several locations, including Chagos, Egypt, Madagascar, Mayotte, Saudi
Arabia, and Tanzania. Additionally, a few site-specific surveys within
these countries' waters noted an absence of the species; however, the
species was still present in other survey locations within those
countries. For example, while H. nobilis was not found during surveys
at Eel Gardens, Egypt, in 2003 or 2006 (Hasan & Abd El-Rady, 2012), the
species was recorded as having a population density of 0.66 individuals
per hectare (indv ha<SUP>-1</SUP>) for Egypt in 2004 (Lawrence et al.
2004), and there are anecdotal data that the species is still commonly
seen by divers (FAO 2019). Thus, where there are available species-
specific data, those data are largely insufficient to support any firm
conclusions regarding the species's status within these locations.
Most of the available data only provide snap-shots of the species
(e.g, density at a certain location and point in time) and do not allow
for species-specific trend analyses across most of H. nobilis' range.
Additionally, where data do indicate declines of H. nobilis, there are
insufficient data on what H. nobilis densities should be to ensure
reproductive success and sustainable populations. For example, in
Chagos, the mean density of H. nobilis reported for Salomon Atoll
declined from 83 ind. ha-1 in 2002 to 10 ind. ha-1 in 2006, with the
authors of the survey indicating concern for the species. Yet, the mean
density for the Seychelles was reported as 2.0 ind. ha-1, with this
population considered to be under exploited (Aumeeruddy & Conand 2008).
However, for most of the range, specifically 18 of the 25 countries
where H. nobilis is reported to occur, species-specific information on
the current as well as historical densities is are unknown.
Although H. nobilis is considered a `high value' species, reliable
catch and trade data for H. nobilis are limited. Most of the available
data are not species specific but pertain to sea cucumbers, in general,
which includes approximately 1700 extant species, making it difficult
to parse out or determine the impacts of threats on H. nobilis and
current status. Additionally, we could not find catch or trade data
that show H. nobilis is the main species targeted throughout its range.
In the Maldives and Mozambique, it is reported that H. nobilis is one
of the top three fished sea cucumber species. In Oman, H. scabra was
the main targeted sea cucumber species, and in Madagascar H. nobilis is
only thought to be ``limitedly harvested'' with H. fuscogilva the
targeted species.
Furthermore, our ability to make reliable predictions of the
impacts of threats and H. nobilis' response into the future is limited
by the variability in not only the quantity and quality of available
data across the species' range regarding its occurrence and the
potential impacts to the species from ongoing and predicted threats,
but also by the high amount of uncertainty regarding how H. nobilis may
respond to those threats, given that the demographic information for
this species is severely limited. We recognize that a number of sea
cucumbers are overfished, but being overfished is not necessarily
equivalent to being at risk of extinction.
Given the limitations of the available data, including sparse
species-specific information hindering status and trend analyses,
significant uncertainty regarding the identification and magnitude of
potential threats to the species throughout most of its range, and a
lack of demographic data to assess how H. nobilis is or may respond to
these threats, we are unable to determine, with any confidence, the
impact of identified potential threats on the status of the species
presently or in the foreseeable future. Thus, we find that the best
available commercial and scientific data available do not support a
conclusion that H. nobilis is at moderate or high risk of extinction
currently or in the foreseeable future.
Significant Portion of Its Range
Under the ESA, a species may be listed if it is in danger of
extinction or likely to become so within the foreseeable future
throughout all or a
[[Page 68484]]
significant portion of its range. Although the available data do not
support a conclusion that H. nobilis is at risk of extinction currently
or in the foreseeable future based on the rangewide assessment, we
examined whether there are any portions of the species' range where H.
nobilis may be facing elevated extinction risk, and whether any such
portions qualify as ``significant portions'' in order to determine
whether the species may qualify for listing on the basis of its status
within a portion of its range.
The Final Policy on Interpretation of the Phrase ``Significant
Portion of Its Range'' in the Endangered Species Act's Definitions of
``Endangered Species'' and ``Threatened Species''(``SPR Policy,'' 79 FR
37578, July 1, 2014), partially guided this assessment. Under the SPR
Policy, we must determine whether there is substantial information
indicating that (1) any portions may be ``significant'' and (2) the
species may be in danger of extinction in those portions or likely to
become so within the foreseeable future. The order in which these
determinations are made is flexible and typically determined based on
the nature of the available information or circumstances for the
particular species.
We note that the definition of ``significant'' in the SPR Policy
has been invalidated in two District Court cases that addressed listing
decisions made by the USFWS. The SPR Policy set out a biologically-
based definition that examined the contributions of the members in the
portion to the species as a whole, and established a specific threshold
(i.e., when the loss of the members in the portion would cause the
overall species to become threatened or endangered). The courts
invalidated the threshold component of the definition because it set
too high a standard. Specifically, the courts held that, under the
threshold in the policy, a species would never be listed based on the
status of the species in the portion, because in order for a portion to
meet the threshold, the species would be threatened or endangered
rangewide. Center for Biological Diversity, et al. v. Jewell, 248 F.
Supp. 3d 946, 958 (D. Ariz. 2017); Desert Survivors v. DOI 321 F. Supp.
3d. 1011 (N.D. Cal., 2018). NMFS did not rely on the definition of
``significant'' in the policy when making this 12-month finding. NMFS
instead examined information relevant to making the second
determination by considering whether there may be a concentration of
threats in portions of the range and whether the species is at risk of
extinction within those portions. When evaluating the threats that H.
nobilis faces, we considered overutilization for international trade in
b[ecirc]che-de-mer and the lack of enforcement of existing regulatory
mechanisms. These two factors are considered the main threats likely
causing negative impacts to H. nobilis at the population level in at
least some portions of its range (see Table 4 in NMFS 2021).
Based on our review of the available data, these main threats
appear to be largely widespread throughout H. nobilis' range. Sea
cucumbers in general face the threats of overutilization and illegal
harvest for the purpose of supplying b[ecirc]che-de-mer to Asian
markets. This demand is ubiquitous throughout the western Indian Ocean
(i.e. the range of H. nobilis; see Figures 8 and 10 in NMFS 2021).
Given the wide-spread nature of these threats, we next considered
whether the species may be responding differently in certain portions
of its range to the point where it may be at risk of extinction from
these threats within those portions.
Where species-specific information is available, the data show
potential negative responses, as evidenced by population declines, in
Chagos, Egypt, Madagascar, Mayotte, Saudi Arabia, and Tanzania.
However, as stated previously in the extinction risk analysis, where
data do indicate species-specific declines there is insufficient data
to indicate the species is facing a risk of extinction in those
locations. For example, in Chagos the mean density reported for Salomon
atoll in 2002 was 83 ind. ha-1 and in 2006 was reported as 10 ind. ha-
1. Although this decline to 10 ind. ha-1 could potentially be a cause
for concern, in the nearby Seychelles, a mean density of 2.0 ind. ha-1,
reported during a 2003-2004 survey, was considered to represent an
underexploited H. nobilis population. Additionally, there are only
anecdotal data for declines in Tanzania and Madagascar. Without
additional information on minimum density thresholds or the
reproductive potential or current productivity of H. nobilis, the
available information does not allow us to conclude that these
populations may be in danger of extinction. Furthermore, sea cucumber
fishing is currently prohibited in Egypt (first in 2001-2002 and
reinstated in 2003), Mayotte (since 2004), Saudi Arabia (since 2006)
and Tanzania (since 2006). While illegal and unregulated fishing is an
issue for sea cucumbers, these fishing bans should be reducing fishing
pressure on the species, and, thus, potentially decreasing the
species's risk of extinction in these areas.
While there are limited data on the locations listed above,
demographic data to determine how H. nobilis may be responding to these
threats are largely lacking. As a result, we are unable to determine
the extinction risk of H. nobilis in any portion of its range. Thus, we
are unable to conclude that the species may be at a moderate or high
risk of extinction in any portion of its range or likely to become so
within the foreseeable future. Because we have made this determination,
we did not separately examine whether any portions qualify as
``significant.'' Furthermore, such an analysis would likely be
challenged by the same type of data limitations, such as lack of
understanding of population structure, population connectivity, and
species-specific abundance data, and as a result, prevent a conclusion
regarding whether any portions are biologically important such that
they qualify as ``significant portions'' of the species' range.
Final Listing Determination
Section 4(b)(1) of the ESA requires that NMFS make listing
determinations based solely on the best scientific and commercial data
available after conducting a review of the status of the species and
taking into account those efforts, if any, being made by any state or
foreign nation, or political subdivisions thereof, to protect and
conserve the species. We have independently reviewed the best available
scientific and commercial information, including the petitions, public
comments submitted on the 90-day finding (85 FR 48144, August 10,
2020), the Status Review Report (NMFS 2021), and other published and
unpublished information. We considered each of the statutory factors to
determine whether each contributed significantly to the extinction risk
of the species. As previously explained, we could not identify a
significant portion of the species's range that is threatened or
endangered. Therefore, our determination is based on a synthesis and
integration of the foregoing information, factors and considerations,
and their effects on the status of the species throughout its entire
range.
We have determined the species does not warrant listing at this
time. This finding is consistent with the statute's requirement to base
our findings on the best scientific and commercial data available.
Given the limitations of the available data, including sparse species-
specific information hindering status and trend analyses, significant
uncertainty regarding the identification and magnitude of potential
threats to the species throughout most of its range,
[[Page 68485]]
and a lack of demographic data to assess how H. nobilis is or may
respond to these threats, we are unable to determine, with any
confidence, the impact of the identified threats on the status of the
species presently or in the foreseeable future. Therefore, H. nobilis
does not meet the definition of a threatened species or an endangered
species and does not warrant listing as threatened or endangered at
this time.
This is a final action, and, therefore, we are not soliciting
public comments.
References
A complete list of the references used in this 12-month finding is
available at <a href="https://www.fisheries.noaa.gov/species/black-teatfish#conservation-management">https://www.fisheries.noaa.gov/species/black-teatfish#conservation-management</a> and upon request (see FOR FURTHER
INFORMATION CONTACT).
Peer Review
In December 2004, the Office of Management and Budget (OMB) issued
a Final Information Quality Bulletin for Peer Review establishing
minimum peer review standards, a transparent process for public
disclosure of peer review planning, and opportunities for public
participation. The OMB Bulletin, implemented under the Information
Quality Act (Pub. L. 106-554) is intended to enhance the quality and
credibility of the Federal Government's scientific information, and
applies to influential or highly influential scientific information
disseminated on or after June 16, 2005. To satisfy our requirements
under the OMB Bulletin, we obtained independent peer review of the
Status Review Report. Three independent specialists were selected from
the academic and scientific community for this review. All peer
reviewer comments were addressed prior to dissemination of the final
Status Review Report and publication of this 12-month finding.
The Peer Review Report can be found online at: <a href="https://www.noaa.gov/organization/information-technology/information-quality-peer-review-id422">https://www.noaa.gov/organization/information-technology/information-quality-peer-review-id422</a>.
Authority
The authority for this action is the Endangered Species Act of
1973, as amended (16 U.S.C. 1531 et seq.).
Dated: November 29, 2021.
Samuel D. Rauch, III,
Deputy Assistant Administrator for Regulatory Programs, National Marine
Fisheries Service.
[FR Doc. 2021-26178 Filed 12-1-21; 8:45 am]
BILLING CODE 3510-22-P
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