Endangered and Threatened Wildlife and Plants; 12-Month Finding on a Petition To List the Black Teatfish (Holothuria nobilis

CourtNational Oceanic And Atmospheric Administration
Citation86 FR 68477
Publication Date02 December 2021
Record Number2021-26178
Federal Register, Volume 86 Issue 229 (Thursday, December 2, 2021)
[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 (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
                

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