Endangered and Threatened Wildlife and Plants; 12-Month Finding on a Petition To List the Black Teatfish (Holothuria nobilis, 68477-68485 [2021-26178]

Agencies

• DEPARTMENT OF COMMERCE
• National Oceanic and Atmospheric Administration

[Federal Register Volume 86, Number 229 (Thursday, December 2, 2021)]
[Notices]
[Pages 68477-68485]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[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: https://www.fisheries.noaa.gov/species/black-teatfish#conservation-management.

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:
     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:
     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
     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:
     0 (no confidence) = No information;
     1 (low confidence) = Very limited information;
     2 (medium confidence) = Some reliable information 
available, but reasonable inference and extrapolation required; and
     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-1 to 
10 ind. ha-1 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-1 and 1.3 ind. 
ha-1 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-1) 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 https://www.fisheries.noaa.gov/species/black-teatfish#conservation-management 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: https://www.noaa.gov/organization/information-technology/information-quality-peer-review-id422.

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