[Federal Register Volume 79, Number 169 (Tuesday, September 2, 2014)]
[Proposed Rules]
[Pages 51929-51942]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: 2014-20811]



National Oceanic and Atmospheric Administration

50 CFR Part 223

[Docket No. 1206013326-4677-02]
RIN 0648-XA984

Endangered and Threatened Wildlife and Plants: Notice of 12-Month 
Finding on a Petition To List the Nassau Grouper as Threatened or 
Endangered Under the Endangered Species Act (ESA)

AGENCY: National Marine Fisheries Service (NMFS), National Oceanic and 
Atmospheric Administration (NOAA), Commerce.

ACTION: Proposed rule; request for comments.


SUMMARY: We, NMFS, announce a 12-month finding and listing 
determination on a petition to list the Nassau grouper (Epinephelus 
striatus) as threatened or endangered under the Endangered Species Act 
(ESA). We have completed a status review of the Nassau grouper in 
response to a petition submitted by

[[Page 51930]]

WildEarth Guardians. After reviewing the best scientific and commercial 
data available, we have determined that the Nassau grouper meets the 
definition of a threatened species. While the species still occupies 
its historical range, spawning aggregations have been reduced in size 
and number due to fishing pressure. The lack of adequate management 
measures to protect these aggregations increases the extinction risk of 
Nassau grouper. Based on these considerations, described in more detail 
in this proposed rule, we conclude that the Nassau grouper is not 
currently in danger of extinction throughout all or a significant 
portion of its range, but is likely to become so within the foreseeable 
future. We are soliciting information that may be relevant to inform 
the final listing and designation of critical habitat.

DATES: Information and comments on the subject action must be received 
by December 31, 2014.

ADDRESSES: You may submit comments, information, or data on this 
document, identified by the code NOAA-NMFS-2014-0101, by any of the 
following methods:
     Electronic Submissions: Submit all electronic comments via 
the Federal eRulemaking Portal. Go to www.regulations.gov/#!docketDetail;D=NOAA-NMFS-2014-0101, click the ``Comment Now!'' icon, 
complete the required fields, and enter or attach your comments.
     Facsimile (fax): 727-824-5309.
     Mail: NMFS, Southeast Regional Office, 263 13th Avenue 
South, St. Petersburg, FL 33701.
     Hand delivery: You may hand deliver written information to 
our office during normal business hours at the street address given 
    The Nassau grouper Biological Report and reference list are 
available by submitting a request to the Species Conservation Branch 
Chief, Protected Resources Division, NMFS Southeast Regional Office, 
263 13th Avenue South, St. Petersburg, FL 33701-5505, Attn: Nassau 
Grouper 12-month Finding. The report and references are also available 
electronically at: http://sero.nmfs.noaa.gov/protected_resources/listing_petitions/index.html.

FOR FURTHER INFORMATION CONTACT: Jason Rueter, NMFS, Southeast Regional 
Office (727) 824-5350; or Lisa Manning, NMFS, Office of Protected 
Resources (301) 427-8466.



    On September 3, 2010, we received a petition from the WildEarth 
Guardians to list speckled hind (Epinephelus drummondhayi), goliath 
grouper (E. itajara), and Nassau grouper (E. striatus) as threatened or 
endangered under the ESA. Due to the scope of the WildEarth Guardians' 
petition, as well as the breadth and extent of the required evaluation 
and response, we provided species-specific 90-day findings in response 
to the petition. The petition asserted that the present or threatened 
destruction, modification, or curtailment of habitat or range; 
overutilization for commercial, recreational, scientific, or 
educational purposes; inadequacy of existing regulatory mechanisms; and 
other natural or manmade factors are affecting its continued existence 
and contributing to the Nassau grouper's imperiled status. The 
petitioner also requested that critical habitat be designated for this 
species concurrent with listing under the ESA.
    On October 10, 2012, we published a 90-day finding for Nassau 
grouper with our determination that the petition presented substantial 
scientific and commercial information indicating that the petitioned 
action may be warranted (77 FR 61559). We also requested scientific and 
commercial information from the public to inform a status report of the 
species including: (1) Status of historical and current spawning 
aggregation sites; (2) historical and current distribution, abundance, 
and population trends; (3) biological information (life history, 
genetics, population connectivity, etc.); (4) management measures, 
regulatory mechanisms designed to protect spawning aggregations, and 
enforcement information; (5) any current or planned activities that may 
adversely impact the species; and (6) ongoing or planned efforts to 
protect and restore the species and its habitat. We received 
information from the public in response to the 90-day finding and 
incorporated the information in the Biological Report and in this 
proposed rule.

Listing Determinations Under the ESA

    We are responsible for determining whether the Nassau grouper is 
threatened or endangered under the ESA (16 U.S.C. 1531 et seq.). 
Section 4(b)(1)(A) of the ESA requires us to make listing 
determinations based solely on the best scientific and commercial data 
available after conducting a review of the status of the species and 
after taking into account efforts being made by any state or foreign 
nation to protect the species. 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 taxonomic species and ``any 
subspecies of fish, or wildlife, or plants, and any distinct population 
segment of any species of vertebrate fish or wildlife which interbreeds 
when mature.'' Under section 4(a) of the ESA, we must determine whether 
any species is endangered or threatened due to 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 (sections 4(a)(1)(A) through (E)).
    To determine whether the Nassau grouper warrants listing under the 
ESA, we first completed a Biological Report, which summarizes the 
taxonomy, distribution, abundance, life history and biology of the 
species (Hill and Sadovy de Mitcheson 2013). The Biological Report also 
identifies threats or stressors affecting the status of the species as 
well as a description of the fisheries, fisheries management, and 
conservation efforts. The Biological Report incorporates information 
received in response to our request for information (77 FR 61559, 
October 10, 2012) and comments from three independent peer reviewers. 
Information from the Biological Report is summarized below under 
``Biological Review.''
    Next, we used the Biological Report to complete a threats 
evaluation and an extinction risk analysis (ERA) to determine the 
status of the species. The results of the threats evaluation are 
discussed below under ``Threats Evaluation'' and the results of the ERA 
are discussed below under ``Results of Extinction Risk Analysis.''
    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.'' Thus, we 
interpret an ``endangered species'' to be one that is presently in 
danger of extinction. A ``threatened species,'' on the other hand, is 
not currently at risk of extinction but is likely to become so in the 
foreseeable future. In other words, a key statutory difference between 
a threatened and endangered species is the timing of when a species may 
be in danger of extinction, either presently (endangered) or in the 
foreseeable future (threatened).

[[Page 51931]]

    In determining whether the species meets the standard of endangered 
or threatened, we considered the specific life history and ecology of 
the species, the nature of threats, the species' response to those 
threats, and population numbers and trends. We considered both the data 
and information summarized in the Biological Report as well as the 
results of the extinction risk analysis. We considered each threat 
identified, both individually and cumulatively. For purposes of our 
analysis, the mere identification of factors that could impact a 
species negatively is not sufficient to compel a finding that ESA 
listing is appropriate. In considering those factors that might 
constitute threats, we look beyond mere exposure of the species to the 
factor to determine whether the species responds, either to a single or 
multiple threats, in a way that causes actual impacts at the species 
level. In making this finding, we have considered and evaluated the 
best available scientific and commercial information, including 
information received in response to our 90-day finding.

Biological Review

    This section provides a summary of key biological information 
presented in the Biological Report (Hill and Sadovy de Mitcheson 2013).

Species Description

    The Nassau grouper, Epinephelus striatus (Bloch 1792), is a long-
lived, moderate sized Serranid fish with large eyes and a robust body. 
The range of color is wide, but ground color is generally buff, with 5 
dark brown vertical bars and a large black saddle blotch on top of 
caudal peduncle and a row of black spots below and behind eye. Color 
pattern can change within minutes from almost white to bicolored to 
uniformly dark brown, according to the behavioral state of the fish 
(Longley 1917, Colin 1992, Heemstra and Randall 1993, Carter et al. 
1994). A distinctive bicolored pattern is seen when two adults or an 
adult and large juvenile meet and is frequently observed in spawning 
aggregations (Heemstra and Randall 1993). There is also a distinctive 
dark tuning-fork mark beginning at the front of the upper jaw, 
extending dorsally (on top) along the interorbital region, and then 
dividing into two branches on top of the head behind the eyes; another 
dark band from the tip of the snout through the eye and then curving 
upward to meet its fellow just before the dorsal-fin origin. Juveniles 
exhibit a color pattern similar to adults (e.g., Silva Lee 1977).
    Maximum age has been estimated up to 29 years, based on an ageing 
study using sagittal otoliths (Bush et al. 2006). Most studies also 
indicate rapid growth, which has been estimated to be about 10 mm/month 
(total length (TL)) for small juveniles, and 8.4 to 11.7 mm/month for 
larger juveniles (30-270 mm TL; Beets and Hixon 1994, Eggleston 1995). 
Maximum size is about 122 cm TL and maximum weight is about 25 kg 
(Heemstra and Randall 1993, Humann and Deloach 2002, Froese and Pauly 
2010). Generation time (the average age of parents in the population) 
is estimated as 9-10 years (Sadovy and Colin 1995).


    The Nassau grouper's confirmed distribution currently includes 
``Bermuda and Florida (USA), throughout the Bahamas and Caribbean Sea'' 
(e.g., Heemstra and Randall 1993). The occurrence of E. striatus from 
the Brazilian coast south of the equator as reported in Heemstra and 
Randall (1993) is ``unsubstantiated'' (Craig et al. 2011). The Nassau 
grouper has been documented in the western Gulf of Mexico, at Arrecife 
Alacranes (north of Progreso) to the west off the Yucatan Peninsula, 
Mexico, (Hildebrand et al. 1964). Nassau grouper is generally replaced 
ecologically in the eastern Gulf by red grouper (E. morio) (Smith 1971) 
in areas north of Key West or the Tortugas. They are considered a rare 
or transient species off Texas in the northwestern Gulf of Mexico 
(Gunter and Knapp 1951 in Hoese and Moore 1977). The first confirmed 
sighting of Nassau grouper in the Flower Garden Banks National Marine 
Sanctuary, which is located in the northwest Gulf of Mexico 
approximately 180 km southeast of Galveston, Texas, was reported by 
Foley et al. (2007). Many earlier reports of Nassau grouper up the 
Atlantic coast to North Carolina have not been confirmed. The 
Biological Report (Hill and Sadovy de Mitcheson, 2013) provides a 
detailed description.

Habitat and Depth

    The Nassau grouper is primarily a shallow-water, insular fish 
species that has long been valued as a major fishery resource 
throughout the wider Caribbean, South Florida, Bermuda and the Bahamas 
(Carter et al. 1994). The Nassau grouper is considered a reef fish, but 
it transitions through a series of developmental shifts in habitat. As 
larvae, they are planktonic. After an average of 35-40 days and at an 
average size of 32 mm TL, larvae recruit from an oceanic environment 
into demersal habitats (Colin 1992, Eggleston 1995). Following 
settlement, Nassau grouper juveniles are reported to inhabit macroalgae 
(primarily Laurencia spp.), coral clumps (Porites spp.), and seagrass 
beds (Eggleston 1995, Dahlgren 1998). Recently-settled Nassau grouper 
have also been collected from tilefish (Malacanthus plumieri) and 
rubble mounds at 18 m depth(Colin et al. 1997). Post-settlement, small 
Nassau grouper have been reported with discarded queen conch shells 
(Strombus gigas) and other debris around Thalassia beds (Randall 1983, 
Eggleston 1995).
    Juvenile Nassau grouper (120-150 mm TL) are relatively solitary and 
remain in specific areas for months (Bardach 1958). Juveniles of this 
size class are associated with macroalgae, and both natural and 
artificial reef structure. As juveniles grow, they move progressively 
to deeper areas and offshore reefs (Tucker et al. 1993, Colin et al. 
1997). Schools of 30-40 juveniles (250-350 mm TL) were observed at 8-10 
m depths in the Cayman Islands (Tucker et al. 1993). No clear 
distinction can be made between types of adult and juvenile habitats, 
although a general size segregation with depth occurs--with smaller 
Nassau grouper in shallow inshore waters (2 to 9 fathoms) and larger 
individuals more common on deeper (10 to 30 fathoms) offshore banks 
(Bardach et al. 1958, Cervig[oacute]n 1966, Silva Lee 1974, Radakov et 
al. 1975, Thompson and Munro 1978).
    Recent work by Nemeth and coworkers in the U.S. Virgin Islands 
(U.S.V.I.; manuscript, in prep) found more overlap in home ranges of 
smaller juveniles compared to larger juveniles, and adults having 
larger home ranges with less overlap. Mean home range of adult Nassau 
grouper in the Bahamas was 18,305m\2\ +/-5,806 (SD) with larger ranges 
at less structurally complex reefs (Bolden 2001). The availability of 
habitat and prey was found to significantly influence home range of 
adults (Bolden 2001).
    Adult Nassau grouper tend to be relatively sedentary and are 
generally associated with high relief coral reefs or rocky substrate in 
clear waters to depths of 130 m. Generally adults are most common at 
depths less than 100 m (Hill and Sadovy de Mitcheson, 2013) except when 
at spawning aggregations where they are known to descend to depths of 
255m (Starr et al. 2007).

Diet and Feeding

    Adult Nassau grouper are unspecialized, bottom-dwelling, ambush-
suction predators (Randall 1965, Thompson and Munro 1978). Numerous 
studies describe Nassau

[[Page 51932]]

grouper as piscivorous as adults (Randall and Brock 1960, Randall 1965, 
Randall 1967, Carter et al. 1994, Eggleston et al. 1998). Feeding takes 
place throughout the diel cycle although most fresh food is found in 
stomachs collected in the early morning and at dusk (Randall 1967). 
Young Nassau grouper (20.2-27.2 mm SL) feed on a variety of plankton, 
including pteropods, amphipods, and copepods (Greenwood 1991, Grover et 
al. 1998).

Population Structure and Genetics

    Multiple genetic analyses indicate that there is high gene flow 
throughout the geographic range of the Nassau grouper; however, the 
relative contributions of populations have yet to be determined 
(Hinegardner and Rosen 1972, Hateley 2005). A study of genetic 
population structure in Nassau grouper, using mitochondrial DNA (mtDNA) 
and nuclear microsatellite DNA, revealed no clearly defined population 
substructuring based on samples from Belize, Cuba, Bahamas, and Florida 
(Sedberry et al. 1996). These data indicate that spawning aggregations 
are not exclusively self-recruiting and that the larval stages can 
disperse over great distances; however, the relative importance of 
self-recruitment and larval immigration to local populations is not 
clear (Sedberry et al. 1996). Samples (n = 264) from Belize, Bahamas, 
Turks and Caicos, and Cayman Islands analyzed through enzyme 
electrophoresis had low to intermediate levels of genetic variability 
and provided no evidence for population sub-structuring by sex or 
small-scale spatial distribution, or for macrogeographic stock 
separation (Hateley 2005). These results are consistent with a single 
panmictic population within the northern Caribbean basin with high gene 
flow through the region. Results of an ongoing Ph.D. dissertation using 
more fine-scale genetic techniques may provide a more detailed 
understanding of population structure (Alexis Jackson, Ph.D. research 
in progress, University of California, Santa Cruz).

Reproductive Biology

    The Nassau grouper was originally considered to be a monandric 
protogynous hermaphrodite, meaning males derive from adult females that 
undergo a change in sex (Smith 1971, Claro et al. 1990, Carter et al. 
1994). However, juveniles possess both male and female tissue, 
indicating they can mature directly into either sex (Sadovy and Colin 
1995). Other characteristics such as the strong male/female size 
overlap, the presence of males that develop directly from the juvenile 
phase and the mating system were found to be inconsistent with 
protogyny (Colin 1992, Sadovy and Colin 1995). Therefore, while 
taxonomically similar to other hermaphroditic grouper species, the 
Nassau grouper is primarily considered a gonochore with separate sexes 
(Sadovy and Colin 1995).
    Male and female Nassau grouper typically mature between 400 and 450 
mm SL (440 and 504 mm TL), with most individuals attaining sexual 
maturity by about 500 mm SL (557 mm TL) and about 4-5 years of age, 
although the smallest mature fish recorded in Cuba was a male in the 
360-390 mm TL size class (Claro et al. 1990). The minimum age at sexual 
maturity based on otoliths is between 4 and 8 years (Bush et al. 1996, 
2006) with most fish spawning by age 7+ years (Bush et al. 2006). 
Nassau grouper raised from the egg in captivity matured at just over 2 
years (400-450 mm SL/440-504 mm TL) (Tucker and Woodward 1994). Size, 
rather than age, may be the major determinant of sexual maturation 
(Sadovy and Eklund 1999).
    Fecundity estimates indicate an average fecundity between 3 and 5 
eggs/mg of ripe ovary. Female Nassau grouper from Belize yielded a mean 
relative fecundity of 4.1 eggs/mg ovary weight and a mean total number 
of 4,200,000 oocytes (range = 350,000-6,500,000 for females from 300 to 
700 mm SL) (Carter et al. 1994). Estimated number of eggs in the ripe 
ovary (90.7 g) of a 445 mm SL Nassau grouper from Bermuda was 785,101 
(Bardach et al. 1958). In the U.S.V.I., mean fecundity was 4.97 eggs/mg 
of ovary (s.d. = 2.32) with mean egg production of 4,800,000 eggs 
(Olsen and LaPlace 1979); however, this may be an overestimate as it 
included premature eggs that may not develop. Fecundity estimates were 
also made, based on vitellogenic oocytes only, from Bahamas fish 
producing a mean relative fecundity of 2.9 eggs/mg ripe ovary (s.d. = 
1.09; n = 64) and a mean fecundity of 716,664 (range = 11,724-4,327,440 
for females, 475-686 mm SL). Estimates of oocyte production from 
animals induced to spawn in captivity are closer to those based solely 
on vitellogenic oocyte counts.

Spawning Behavior and Habitat

    Nassau grouper form spawning aggregations at predictable locations 
around the winter full moon, or between full and new moons (Smith 1971, 
Colin 1992, Tucker et al. 1993, Aguilar-Perera 1994, Carter et al. 
1994, Tucker and Woodward 1994). Aggregations consist of hundreds, 
thousands, or, historically, tens of thousands of individuals. Some 
aggregations have persisted at known locations for periods of 90 years 
or more (see references in Hill and Sadovy de Mitcheson 2013). Pair 
spawning has not been observed.
    About 50 individual spawning aggregation sites have been recorded, 
mostly from insular areas in the Bahamas, Belize, Bermuda, British 
Virgin Islands, Cayman Islands, Cuba, Honduras, Jamaica, Mexico, Puerto 
Rico, Turks and Caicos and the U.S.V.I.; however, many of these may no 
longer form (Hill and Sadovy de Mitcheson 2013, Figure 10). Recent 
evidence suggests that spawning is occurring at what appear to be 
reconstituted or novel spawning sites in both Puerto Rico and the 
U.S.V.I. (Hill and Sadovy de Mitcheson 2013). Suspected or anecdotal 
evidence also identifies spawning aggregations in Los Roques, Venezuela 
(Boomhower et al. 2010) and Old Providence in Colombia's San 
Andr[eacute]s Archipelago (Prada et al. 2004). Neither aggregation nor 
spawning has been reported from South America although ripe Nassau 
grouper are frequently caught in certain areas (F. Cervig[oacute]n, 
Fundacion Cientifica Los Roques-Venezuela, pers. comm. to Y. Sadovy, 
NMFS, 1991). Spawning aggregation sites have not been reported in the 
Lesser Antilles, Central America south of Honduras, or Florida.
    ``Spawning runs,'' or movement of adult Nassau grouper from coral 
reefs to spawning aggregations sites, were first described in Nassau 
grouper from Cuba in 1884 by Vilaro Diaz, and later by Guitart-Manday 
and Juarez-Fernandez (1966). Nassau grouper migrate to aggregation 
sites in groups numbering between 25 and 500, moving parallel to the 
coast or along shelf edges or even inshore reefs (Colin 1992, Carter et 
al. 1994, Aguilar-Perera and Aguilar-Davila 1996, Nemeth et al. 2009). 
Distance traveled by Nassau grouper to aggregation sites is highly 
variable with some fish moving only a few kilometers, while others move 
up to several hundred kilometers (Colin 1992, Carter et al. 1994, 
Bolden 2000). Ongoing research in the Exuma Sound, Bahamas has tracked 
migrating Nassau grouper up to 200 km (125 mi), with likely estimates 
of up to 330 km (205 mi), as they move to aggregation sites (Hill and 
Sadovy de Mitcheson 2013).
    Observations suggest that individuals can return to their original 
home reef following spawning. Bolden (2001) reported two tagged fish 
(n=22) returning to home reefs in the Bahamas one year following 
spawning. Sonic tracking studies around Little Cayman Island have 
demonstrated that spawners may return to the aggregation site in 
successive months with returns to their

[[Page 51933]]

residential reefs in between (Semmens et al. 2007). Sixty percent of 
fish tagged at the west end spawning aggregation site in Little Cayman 
in January 2005, returned to the aggregation site in February 2005 
(Semmens et al. 2007). Larger fish are more likely to return to 
aggregation sites and spawn in successive months than smaller fish 
(Semmens et al. 2007).
    It is not known how Nassau grouper select and locate aggregation 
sites or why they aggregate to spawn. Spawning aggregation sites are 
typically located near significant geomorphological features, such as 
projections (promontories) of the reef as little as 50 m from the 
shore, and close to a drop-off into deep water over a wide (6-60 m) 
depth range (Craig 1966, Smith 1972, Burnett-Herkes 1975, Olsen and 
LaPlace 1979, Colin et al. 1987, Carter 1989, Fine 1990, Beets and 
Friedlander 1998, Colin 1992, Aguilar-Perera 1994). Sites are 
characteristically small, highly circumscribed areas, measuring several 
hundred meters in diameter, with soft corals, sponges, stony coral 
outcrops, and sandy depressions (Craig 1966, Smith 1972, Burnett-Herkes 
1975, Olsen and LaPlace 1979, Colin et al. 1987, Carter 1989, Fine 
1990, Beets and Friedlander 1998, Colin 1992, Aguilar-Perera 1994). 
Recent work has identified geomorphological similarities in spawning 
sites that may be useful in applying remote sensing techniques to 
discover previously unknown spawning sites (Kobara and Heyman 2010).
    The link between spawning sites and settlement sites is also not 
well understood. Larval sampling adjacent to a spawning aggregation at 
Mahahual, Mexico (V[aacute]squez-Yeomans et al. 1998) failed to capture 
a single Nassau grouper larva, perhaps due to methodology or the 
density of spawning fish. Researchers speculate the location of 
spawning sites is to assist in offshore transport of fertilized eggs. 
However, currents nearby aggregation sites do not necessarily favor 
offshore egg transport, indicating some locations may be at least 
partially self-recruiting (e.g., Colin 1992). In a similar study around 
a spawning aggregation site at Little Cayman, surface velocity profile 
drifters released on the night of peak spawning showed significant eddy 
formation so that Drifters released nearby an aggregation site at 
Little Cayman remain near or returned to the spawning reef on the night 
of spawning compared to those that moved away on nights preceding 
(Heppell et al. 2011).
    Spawning aggregations usually form between December and March 
(reviewed in Sadovy and Eklund 1999) within the narrow water 
temperature range of 25-26 [deg]C over a wide range of day-lengths 
(Colin 1992, Tucker et al. 1993, Carter et al. 1994). Temperature is 
evidently a more important stimulus for spawning than day length (Hill 
and Sadovy de Mitcheson 2013). In more northerly latitudes (i.e., 
Bermuda), the reproductive season falls between May and August, peaking 
in July (La Gorce 1939, Bardach et al. 1958, Smith 1971, Burnett-Herkes 
1975). Spawning occurs for up to 1.5 hours around the time of sunset 
for several days in each of several months (Whaylen et al. 2007).
    At spawning aggregation sites, Nassau grouper tend to mill around 
for a day or two in a ``staging area'' adjacent to the core area where 
spawning activity actually takes place (Colin 1992, Kadison et al. 
2010, Nemeth 2012). Prior to spawning, individuals milling around over 
the substrate exhibit one of four distinctive color phases: barred 
(normal); bicolor; white belly; or dark phase. There are 
intergradations of these patterns, with rapid changes among patterns 
possible (Colin 1992). Different color phases have also been associated 
with specific times or stages of spawning events (Colin 1992).
    Courtship is indicated by two behaviors which occur late in the 
afternoon: ``following'' and ``circling'' (Colin 1992). ``Following'' 
occurs as one or more fish in the bicolor phase swim closely behind an 
apparent female while ``circling'' occurs as a bicolor phase fish 
circles a barred or dark phase fish. The aggregation then moves into 
deeper water shortly before spawning (Colin 1992, Tucker et al. 1993, 
Carter et al. 1994), by which time all individuals are either ``dark 
phase'' or ``bicolor.'' Progression from courtship to spawning may 
depend on aggregation size, but generally fish move up into the water 
column, with an increasing number exhibiting the bicolor phase (Colin 
1992, Carter et al. 1994).
    Spawning involves a rapid horizontal swim or a ``rush'' of bicolor 
fish following dark fish closely in either a column or cone rising to 
within 20-25 m of the water surface where group-spawning occurs in sub-
groups of 3-25 fish (Olsen and LaPlace 1979, Carter 1986, Aguilar-
Perera and Aguilar-Davila 1996). Then there is release of sperm and 
eggs and a rapid return of the fragmented sub-group to the substrate. 
Similar accounts of spawning behavior from the U.S.V.I. described the 
aggregated fish as a cone in the water column rather than being 
dispersed across the bottom (Olsen and LaPlace 1979). All spawning 
events have been recorded within 20 minutes of sunset and most within 
10 minutes of sunset (Colin 1992).
    Repeated spawning occurs at the same site for up to three 
consecutive months during the correct moon phase. Participation by 
individual fish across the time periods is unknown. It has been 
suggested that individual females spawn repeatedly over several 
different days during one aggregation based on reproductive tissue 
(Smith 1972, Sadovy, NMFS, pers. obs.). Videotape recording shows a 
single female in repeated spawning rushes during a single night, 
indicating repeated release of eggs (Colin 1992). It is unknown whether 
a single, mature female will spawn across the spawning season or even 
each year.

Status Assessments

    Few formal stock assessments have been conducted for the Nassau 
grouper. The most recent published assessment, conducted in the 
Bahamas, indicates fishing effort, and hence fishing mortality (F), in 
the Bahamas needs to be reduced from the 1998-2001 levels, otherwise 
the stocks are likely to be overexploited relative to biological 
reference points (Cheung et al. 2013). The population dynamic modeling 
by Cheung et. al (2013) found: ``assuming that the closure of the 
spawning aggregation season is perfectly implemented and enforced, the 
median value of FSPR (fishing mortality rate that produces a certain 
spawning potential ratio) = 35% on non-spawning fish would be 50% of 
the fishing mortality of the 1998 to 2001 level. The 5% and 95% 
confidence limits are estimated to be less than 20% and more than 100% 
of the fishing mortality at the 1998 to 2001 level, respectively. In 
other words, if (1) fishing mortality (F) rates of non-spawning fish 
are maintained at the 1998 to 2001 level, and (2) fishing on spawning 
aggregations is negligible, the median spawning potential (spawner 
biomass relative to the unexploited level) is expected to be around 25% 
(5 and 95% CI of 20 and 30%, respectively). This level is significantly 
below the reference limit of 35% of spawning potential, meaning that 
there is a high chance of recruitment overfishing because of the low 
spawning stock biomass.''
    The Nassau grouper was formerly one of the most common and 
important commercial groupers in the insular tropical western Atlantic 
and Caribbean (Smith 1978, Randall 1983, Appeldoorn et al. 1987, Sadovy 
1997). Declines in landings and catch per unit of effort (CPUE) have 
been reported throughout its range, and it is now considered to be 
commercially extinct (the species is extinct for fishery purposes due 
to low catch per unit effort) in a number of

[[Page 51934]]

areas, including Jamaica, Dominican Republic, U.S.V.I., and Puerto Rico 
(Sadovy and Eklund 1999). Information on past and present abundance and 
density, at coral reefs and aggregation sites, is based on a 
combination of anecdotal accounts, visual census surveys, and fisheries 
data. Because grouper species are reported collectively in landings 
data, there are limited species-specific data to determine catch of 
Nassau grouper throughout its range.
    While fisheries dependent data are generally limited for the 
species throughout its range, there are some 1970s and 1980s port-
sampling data from the U.S.V.I. and Puerto Rico. In the U.S.V.I., 
Nassau grouper accounted for 22 percent of total grouper landings with 
85 percent of the Nassau grouper catch coming from spawning 
aggregations (D. Olsen, Chief Scientist--St. Thomas Fishermen's 
Association, pers. comm. to J. Rueter, NMFS, October 2013). The first 
U.S. survey of the fishery resources of Puerto Rico noted the Nassau 
grouper was common and a very important food fish, reaching a weight of 
22.7 kg (50 lbs.) or more (Evermann 1900). The Nassau grouper was still 
the fourth-most common shallow-water species landed in Puerto Rico in 
the 1970's (Thompson 1978), and it was common in the reef fish fishery 
of the U.S.V.I. (Olsen and LaPlace 1979). By 1981, ``the Nassau grouper 
ha(d) practically disappeared from the local catches and the ones that 
d(id) appear (were) small compared with previous years'' (CFMC 1985), 
and by 1986, the Nassau grouper was considered commercially extinct in 
the U.S.V.I./Puerto Rico region (Bohnsack et al. 1986). About 1,000 kg 
of Nassau grouper were landed from the Puerto Rico Reef Fish Fishery 
during the latter half of the 1980s, and most of them were less than 
500 mm, indicating they were likely sexually immature (Sadovy 1997).
    A number of organizations and agencies have conducted surveys to 
examine the status of coral reefs and reef fish populations throughout 
the western Atlantic, as well as other parts of the world. Results from 
these monitoring studies offer some indication of relative abundance in 
various locations for Nassau grouper, although different methods are 
often employed and thus results of different studies cannot be directly 
compared (Kellison et al. 2009). The Atlantic and Gulf Rapid Reef 
Assessment Program (AGRRA), which samples a broad spectrum of western 
Atlantic reefs, reports few Nassau groupers with sighting frequency 
(proportion of all surveys with at least one Nassau present) ranging 
from less than 1% to less than 10% per survey from 1997-2000. Densities 
of Nassau grouper range from 1 to 15 fish/hectare with a mean of 5.6 
fish/hectare across all areas surveyed (AGRRA). NOAA's Coral Reef 
Ecosystem Monitoring Program (CREMP) has conducted studies on coral 
reefs in Puerto Rico and the U.S.V.I. since 2000, and sighting 
frequency has ranged from 0 to 0.5% and density has ranged from 0 to 
0.5 fish/hectare. Data from University of the Virgin Islands (UVI Vis. 
Sur.) Self contained underwater breathing apparatus (SCUBA) surveys 
report densities of Nassau grouper at 4 fish/hectare per survey across 
reef habitat types in the U.S.V.I. SCUBA surveys by NOAA in the Florida 
Keys across reef habitat types have sighting frequencies per survey 
between 2-10%; with densities at 1 fish/hectare (NOAA's NMFS FRVC). In 
addition to these surveys, Hodgson and Liebeler (2002) noted that 
Nassau grouper were absent from 82% of shallow Caribbean reefs (3-10m) 
during a 5-year period (1997-2001) of underwater surveys in most 
countries in the range of the species for the ReefCheck project.

Fishing Impacts on Spawning Aggregations

    Historically, fifty spawning aggregation sites had been identified 
throughout the Caribbean (Sadovy de Mitcheson et al. 2008). Of these 
50, less than 20 probably still remain (Sadovy de Mitcheson et al. 
2008). Furthermore, while numbers of fish at aggregation sites [once] 
numbered in the tens of thousands (30,000-100,000 fish; Smith 1972), 
they have now been reduced to less than 3,000 at those sites where 
counts have been made (Sadovy de Mitcheson et al. 2008). Because we 
lack sufficient stock assessments or population estimates, here we use 
spawning aggregation trends as a proxy for population trends. We 
believe the status of spawning aggregations is likely to be reflective 
of the overall population, because adults migrate to spawning 
aggregations for the only known reproductive events.
    In general, slow-growing, long-lived species (such as snappers and 
groupers) with limited spawning periods and, possibly, with only a 
narrow recruitment window are susceptible to overexploitation (Bannerot 
et al. 1987, Polovina and Ralston 1987). The strong appeal of spawning 
aggregations as targets for fishing, their importance in many seasonal 
fisheries, and the apparent abundance of fish at aggregations, make 
spawning aggregations particularly susceptible to over-exploitation. 
There are reports from across the Caribbean where Nassau grouper 
spawning aggregations have repeatedly been discovered, fished, and then 
ceased to exist, or exist at such low densities that spawning fails. 
Nassau grouper were exclusively fished during aggregation formation 
during the 1970's in Bermuda. Commercial landings in 1975 were 75,000 
tons; by 1981, landings had fallen to 10,000 tons (Sadovy de Mitcheson 
and Erisman 2012). The four known spawning aggregation sites ceased to 
form shortly after and have still not recovered (Sadovy de Mitcheson 
and Erisman 2012). In Mahahual, Quintana Roo, Mexico, aggregations of 
up to 15,000 fish formed each year at the same site, but due to 
increased fishing pressure in the 1990's, aggregations have not formed 
since 1996, and management measures designed to protect spawning 
aggregations are not enforced (Aguilar-Perera 2007). Nassau grouper 
were almost exclusively targeted during aggregation formation in Cuba; 
because of this, 20 of the 21 known aggregations no longer form (Claro 
et al. 2009). In Belize there has been an eighty percent decline in the 
last 25 years in size of the Glover's Reef aggregation (15,000 fish to 
3,000). Additionally, only 2 of the 9 known aggregations still formed 
as of 2001, and those had been reduced from 30,000 fish to 1,000-5,000 
fish. Recent work has identified 15 spawning aggregation sites in 
Belize. Seven of these sites were monitored for a ten year period 
(2003-2012). The number of fish counted at all seven sites has remained 
very low (five sites have less than 170 fish, the other two have 1,050 
and 1,350), with no sign of recovery (Belize SPAG workgroup 2012). 
Similar situations are known to have occurred in in the Bahamas, 
U.S.V.I., Puerto Rico, and Honduras (Sadovy de Mitcheson and Erisman 
2012, see also Hill and Sadovy de Mitcheson 2013).
    Further indicators of population decline are the reduced size and/
or age of fish in many of the spawning aggregations that remain. It is 
unusual to obtain individuals of more than 12 years of age in exploited 
fisheries, with more heavily fished areas yielding much younger fish on 
average. The maximum age estimate in the heavily exploited U.S.V.I. 
population is 9 years (Olsen and LaPlace 1979), 12 years in northern 
Cuba, 17 years in southern Cuba (Claro et al. 1990), and 21 years from 
the Bahamas, (Sadovy and Colin 1995). Most individuals caught from a 
U.S.V.I. spawning aggregation were between about 500 and 600 mm TL 
(Olsen and LaPlace 1979). Nemeth et al. (2006) found that adult Nassau 
grouper at a

[[Page 51935]]

different spawning aggregation site (Grammanik Bank) in the U.S.V.I. 
ranged between 480 and 800 mm with average total length for males (603 
mm, n = 18) and females (591 mm, n = 44) being similar.
    While heavy fishing on spawning aggregations may have been a 
primary driver of population declines as reflected by the observed 
declines in spawning aggregations (Sadovy de Mitcheson and Erisman 
2012), other factors may affect abundance. For example, heavy fishing 
of adults away from or during spawning runs, intensive capture of 
juveniles, either through direct targeting (e.g., spearfishing) or 
using small mesh traps or nets, are also occurring (Hill and Sadovy de 
Mitcheson 2013). In addition to the high fishing pressure in some 
areas, poaching also appears to be affecting some populations (e.g., in 
the Cayman Islands, Semmens et al. 2012).

Threats Evaluation

    The threats evaluation was the second step in the process of making 
an ESA listing determination for Nassau grouper as described above in 
``Listing Determinations Under the ESA''. The Extinction Risk Analysis 
Group (ERAG), which consisted of 12 NOAA Fisheries Science Center and 
Regional Office personnel, was asked to independently review the 
Biological Report and assess 4 demographic factors (abundance, growth 
rate/productivity, spatial structure/connectivity, and diversity) and 
13 specific threats (see ERA Threat Table under supporting documents). 
The group members were asked to provide qualitative scores based on 
their perceived severity of each factor and threat.
    The ERAG members were asked to independently evaluate the severity, 
scope, and certainty for these threats currently and in the foreseeable 
future (30 years from now). The foreseeable future was based on our 
consideration of age at maturity, estimated generation time, and 
threats. Using a generation time of 10 years and an age at maturity of 
8 years (Bush et al. 1996, 2006; Legault and Eklund 1998), we chose 30 
years as the foreseeable future time-frame, which would potentially 
allow three generations of mature individuals to contribute to spawning 
aggregations. Given the limited information we have to predict the 
impacts of threats, we felt the 30 year timeframe was the most 
appropriate to predict impacts from threats in the future.
    ERAG members were asked to rank each of four demographic factors 
and 13 identified threats as ``very low risk,'' ``low risk,'' 
``moderate risk,'' ``increasing risk,'' ``high risk,'' or ``unknown.'' 
``Very low risk'' meant that it is unlikely that the demographic factor 
or threat affects the species' overall status. ``Low risk'' meant that 
the demographic factor may affect species' status, but only to a degree 
that it is unlikely that this factor significantly elevates risk of 
extinction now or in the future. ``Moderate risk'' meant that the 
demographic factor or threat contributes significantly to long term 
risk of extinction, but does not constitute a danger of extinction in 
the near future. ``Increasing risk'' meant that the present demographic 
risk or threat is low or moderate, but is likely to increase to high 
risk in the foreseeable future if present conditions continue. Finally, 
``high risk'' meant that the demographic factor or threat indicates 
danger of extinction in the near future. The ERAG evaluated risk on 
this scale, and we then interpreted these rankings against the 
statutory language for threatened or endangered to determine the status 
of Nassau grouper.
    ERAG members were also asked to consider the potential interactions 
among demographic factors and threats. If the demographic factor or 
threat was ranked higher due to interactions with other demographic 
factors or threats, ERAG members were asked to identify those factors 
or threats that caused them to score the risk higher or lower than it 
would have been if it were considered independently. We then examined 
the independent responses from each ERAG member for each demographic 
factor and threat and used the modal response to determine the level of 
threat to Nassau grouper.
    Climate change and international trade regulations (e.g. CITES, as 
described in the Biological Report) were categorized as ``unknown.'' 
Habitat alteration, U.S. federal regulations, disease/parasites/
abnormalities, and aquaculture were ranked as ``very low risk'' to 
``low risk.'' State/territorial regulations, growth rate/productivity, 
abundance, spatial structure/connectivity, commercial harvest, foreign 
regulations, artificial selection, and diversity were ranked as 
``moderate risk'' to ``increasing risk.'' Historical harvest (the 
effect of prior harvest on current population status), spawning 
aggregation fishing, and inadequate law enforcement were classified as 
``high risk.'' The demographic factors and threats are described below 
by the five listing factors with the corresponding ERAG ranking for 
each demographic factor or threat.

A. The Present or Threatened Destruction, Modification, or Curtailment 
of Its Habitat or Range

    Spatial structure/connectivity and habitat alteration were 
considered under Factor A; this included habitat loss or degradation, 
and the loss of habitat patches, critical source populations, 
subpopulations, or dispersal among populations.
    Nassau grouper use many different habitat types within the coral 
reef ecosystem. The increase in urban, industrial, and tourist 
developments throughout the species' range impacts coastal mangroves, 
seagrass beds, estuaries, and live coral (Mahon 1990). Loss of juvenile 
habitat, such as macroalgae, seagrass beds, and mangrove channels is 
likely to negatively affect recruitment rates. Habitat loss or 
degradation was ranked by the ERAG as a ``low risk'' threat to Nassau 
grouper. In conclusion, the use of many different habitat types by 
Nassau grouper greatly reduces a risk of extinction from habitat loss 
or degradation (Hill and Sadovy de Mitcheson 2013).
    As described in Hill and Sadovy de Mitcheson (2013), a study of 
genetic population structure in Nassau grouper revealed no clearly 
defined population substructuring at the geographic locations sampled, 
i.e. Belize, Cuba, Bahamas, and Florida (Sedberry et al. 1996). Based 
on ERAG scores, spatial structure/connectivity was characterized as an 
``increasing'' risk for Nassau grouper. We agree with the ERAG ranking 
and believe this increasing risk is due to the declining number and 
size of spawning aggregations, which affects population structure.

B. Overutilization for Commercial, Recreational, Scientific, or 
Educational Purposes

    Based on ERAG rankings, historical harvest and spawning aggregation 
fishing are two of the three most severe threats (the third being lack 
of law enforcement) to Nassau grouper. Historical harvest and fishing 
spawning aggregations were both classified as ``high'' risk threats to 
Nassau grouper. Curiously, the ERAG rankings for commercial harvest, 
which often includes the fishing on spawning aggregations, were lower 
and indicated current commercial harvest was a ``moderate'' threat for 
Nassau grouper. Current abundance was similarly classified as a 
``moderate'' risk for Nassau grouper.
    Two different aspects of fishing affect Nassau grouper abundance: 

[[Page 51936]]

effort throughout the non-spawning months and directed fishing at 
spawning aggregations or migrating adults. Nassau grouper are fished 
commercially and recreationally throughout the year by handline, 
longline, fish traps, spear guns, and gillnets (NMFS General Canvas 
Landing System). Fishing at aggregations is mainly conducted by 
handlines or by fish traps, although gillnets were being used in Mexico 
in the early to mid-1990s (Aguilar-Perera 2004). Declines in landings, 
catch per unit effort (CPUE) and, by implication, abundance in the late 
1980's and early 1990's occurred throughout its range, which has led 
Nassau grouper to now be considered commercially extinct in a number of 
areas (Sadovy and Eklund 1999). Population declines and loss of 
aggregations continue throughout the Nassau grouper's range (Sadovy de 
Mitcheson 2012).
    These predictable spawning aggregations make Nassau grouper a 
vulnerable fishing target. In many places, annual landings for Nassau 
grouper were mostly from aggregation-fishing (e.g., Claro et al. 1990, 
Bush et al. 2006). Because Nassau grouper are only known to reproduce 
in spawning aggregations, removing ripe individuals from the spawning 
aggregations greatly influences population dynamics and future fishery 
yields (Shapiro 1987). Harvesting a species during its reproductive 
period increases adult mortality and diminishes juvenile recruitment 
rates. The loss of adults and the lack of recruitment greatly increase 
a species' extinction risk. The collapse of aggregations in many 
countries (Sadovy de Mitcheson 2012) may be due to the fact that much 
of the catch in many countries historically came from spawning 
aggregations (Olsen and LePlace 1978, Aguilar-Perera 1994, Sadovy and 
Eklund 1999). As Semmens et al. (2012) noted from the results of a 
mark-recapture study on Cayman Brac, Cayman Island fishermen appear to 
catch sufficient adult grouper outside the spawning season to seriously 
impact populations. It appears that aggregation fishing has led to such 
depressed populations that fishing operations away from the 
aggregations are impacting the status of the populations.
    The final threat analyzed for Factor B was artificial selection. 
The ERAG scores indicated artificial selection was a ``moderate'' 
threat; however, ranking of this threat was widely distributed amongst 
ERAG members, indicating a high level of uncertainty about the effects 
of artificial selection on Nassau grouper.

C. Disease and Predation

    There is very little information on the impacts of disease, 
parasites, and abnormalities on Nassau grouper, but Nassau grouper are 
not known to be affected by any specific disease or parasite. 
Additionally, Nassau grouper are not known to be at an increased risk 
of extinction due to predation. The ERAG ranking indicated a ``very low 
risk'' threat from disease, parasites, and predation.

D. Inadequacy of Existing Regulatory Mechanisms

    The inadequacy of existing regulatory mechanisms, including 
inadequate law enforcement, international trade regulations, foreign 
nations' domestic laws, U.S. federal laws, and U.S. state and 
territorial laws were considered under Factor D. The lack of law 
enforcement was noted by members of the ERAG as influencing their 
scoring for abundance, fishing spawning aggregations, commercial 
harvest, and historical harvest. The lack of law enforcement lead to 
higher risk scores for these threats. Inadequate law enforcement was 
ranked as a ``high risk'' to Nassau grouper. Rankings for the other 
categories of regulatory mechanisms were widely distributed, with only 
one considered an ``increasing'' risk (foreign regulations). The 
remaining two categories of regulations (U.S. federal and State of 
Florida and U.S. territory regulations) were considered ``low risk'' to 
``moderate risk.'' While the ERAG ranking for regulatory mechanisms 
were generally low, the concern about fishing spawning aggregations 
(``high risk'') may be in part due to regulatory mechanisms.

Summary of Existing Regulatory Mechanisms

    As discussed in detail in the Biological Report (Hill and Sadovy de 
Mitcheson 2013), a wide array of regulatory mechanisms exists 
throughout the range of Nassau grouper that are intended to limit 
harvest. Existing regulatory mechanisms include minimum sizes 
restrictions, seasonal closures, spatial closures, and gear and access 
restrictions. We summarize some of these regulatory mechanisms below by 
    In the 1980s, the Bahamas introduced a minimum size of 3 lbs. (1.36 
kg) for Nassau grouper. This was followed in 1998 with a 10-day 
seasonal closure at several spawning aggregations. An annual ``two-
month'' fishery closure was added in December 2003 to coincide with the 
spawning period and was extended to three months in 2005 to encompass 
the December through February spawning period. The 3-month closure 
implementation is determined annually and could be shortened or 
otherwise influenced by such factors as the economy (Sadovy and Eklund 
1999). During the 3-month closure there is a national ban on Nassau 
grouper catches; however, the Bahamas Reef Educational Foundation 
(BREEF; unpub. data), has reported large numbers of fish being taken 
according to fisher accounts with photo-documentation and confirming 
reports of poaching of the species during the aggregation season.
    There are marine parks in the Bahamas that are closed to fishing 
and therefore protect Nassau grouper. The Exuma Cays Land and Sea Park, 
first established in 1959, has been closed to fishing since 1986, thus 
protecting both nursery and adult habitat for Nassau grouper and other 
depleted marine species. Other sites, including the South Berry Islands 
Marine Reserve (established on December 29, 2008), Southwest New 
Providence National Park, and North Exumas Study Site have also been 
established and closed to fishing. Several gear restrictions are 
protective of Nassau grouper. Fishing with SCUBA and the use of 
explosives, poisons, and spearguns is prohibited in the Bahamas, 
although snorkeling with sling spears is allowed. The use of bleach or 
other noxious or poisonous substances for fishing, or possession of 
such substances on board a fishing vessel, without written approval of 
the Minister, is prohibited. Commercial fishing in the Bahamas is 
restricted to only the native population and, as a consequence, all 
vessels fishing within the Bahamas Exclusive Fishery Zone must be fully 
owned by a Bahamian citizen residing in the Bahamas.
    In Belize, the first measure to protect Nassau grouper was a 
seasonal closure within the Glover's Reef Marine Reserve in 1993; the 
area was closed from December 1 to March 1 to protect spawning 
aggregations. A seasonal closure zone to protect Nassau grouper 
spawning aggregations was included when the Bacalar Chico marine 
reserve was established in 1996 (Paz and Truly 2007). Minimum and 
maximum capture sizes were introduced a decade ago (see Hill and Sadovy 
de Mitcheson 2013, Sala et al. 2001, Carter et al. 1994, Heyman and 
Requena 2002, Sadovy de Mitcheson et al. 2008; J. Gibson, Wildlife 
Conservation Society--Belize City, Belize, pers. comm. to Y. Sadovy, 
University Hong Kong, 2010).
    In 2001 the Belize National Spawning Aggregation Working Group 
established protective legislation for 11 of the

[[Page 51937]]

known Nassau grouper spawning sites. Seven of those 11 sites are 
monitored as regularly as possible. The Working Group meets regularly 
to share data and develop management strategies (www.spagbelize.org; 
retrieved on 15 April 2012) and monitoring continues at several sites. 
In 2003, Belize introduced a four-month closed season to protect 
spawning fish (O'Connor 2002, Gibson 2008). However, the legislation 
introduced in 2003 allowed for exemptions to the closures by special 
license granted by the Fisheries Administrator. These special licenses 
made it difficult to enforce the national prohibition and in 2010, 
Belize stopped issuing fishers permits to fish for Nassau grouper 
during the 4-month spawning period, except at Maugre Caye and Northern 
Two Caye.
    Belize issued additional protective measures in early April 2009 to 
help manage and protect the Nassau grouper. These include minimum and 
maximum size limits of 510 mm (20 inches) and 760 mm (30 inches), 
respectively, and a planned ban on all spear fishing within all marine 
reserves (yet to be implemented). Furthermore, as a large proportion of 
finfish are landed as fillets, the new regulations require that all 
Nassau grouper be landed whole, and if filleted must have a 1-2 inch 
(25-50 mm) skin patch (The Belize Spawning Aggregation Working Group 
2009). Other gear restrictions are in place for reef fishes generally 
to aid in their management, such as no spearfishing on compressed air.
    Although Bermuda closed red hind aggregation sites in 1974, Nassau 
grouper aggregation sites located seaward of these sites were not 
protected and continued to be fished. In 1990, a two-fish bag limit and 
minimum size restriction (356 mm FL) were enacted in Bermuda (Luckhurst 
1996). Since 1996, Nassau grouper has been completely protected through 
a prohibition on take and possession and likely benefits from numerous 
no-take marine reserves (Hill and Sadovy de Mitcheson 2013).
    In the late 1970s (Hill and Sadovy de Mitcheson 2013), the three 
main (``traditional'') grouper ``holes'' in the Cayman Islands were 
officially protected and only residents were allowed to fish by lines 
during spawning season. In 1986, increasing complaints from fishermen 
of a decline in both numbers and size of Nassau grouper taken from the 
fishery prompted the implementation of a monitoring program by the 
Department of the Environment (Bush et al. 2006).
    In 1998, these three main grouper holes at the eastern ends of the 
islands were formally designated as ``Restricted Marine Areas'' for 
which access required licensing by the Marine Conservation Board (the 
statutory authority responsible for the administration of the Marine 
Conservation Law) (Bush et al. 2006). In the early 1990s, legislation 
prohibited spearfishing at spawning aggregation sites. In February 
2002, protective legislation defined a spawning season as November 1 to 
March 31, and an ``Alternate Year Fishing'' rule was passed. This law 
allowed fishing of the spawning aggregations to occur every other year 
with the first non-fishing year starting in 2003, and also set a catch 
limit of 12 Nassau grouper per boat per day during fishing years. The 
law defined the one nautical mile (nm) ``no trapping'' zones around 
each spawning site, and set a minimum size limit of 12 inches for 
Nassau grouper in 2002 in response to juveniles being taken by fish 
traps inside the sounds (Whaylen et al. 2004, Bush et al. 2006). In 
2003, spearguns were restricted from use within 1 nautical mile of any 
designated grouper spawning area from November through March. In 2008, 
it was prohibited to take any Nassau grouper by speargun anywhere in 
Cayman waters. Effective December 29, 2003, the Marine Conservation 
Board, closed fishing at all designated Nassau grouper spawning sites 
for a period of 8 years. The conservation measure was renewed for a 
further 8 years in 2011.
    In Cuba, there is a minimum size of 32 cm TL (or 570 g) for Nassau 
grouper. This is not protective because the size of maturity is 48 cm 
TL. Of some benefit to Nassau grouper are bag limits for recreational 
fishing, regulations to increase selectivity of fishing gears to avoid 
the catch of juveniles, limits of net use during spawning aggregation 
time, and controls of speargun use, both commercially and 
recreationally. Marine protected areas have been introduced throughout 
the country. In 2002, the total number of recreational licenses was 
limited to 3,500 for the whole country hoping to reduce directed 
fishing pressure.
    In Mexico, following scientific documentation of declines of Nassau 
grouper at Mahahual (Aguilar-Perera 1994), two regulations were 
enacted: 1) spear-fishing was banned at any spawning aggregation sites 
in southern Quintana Roo in 1993; and 2) in 1997 the fishing of any 
grouper species was banned during December and January (Aguilar-Perera 
2006). In 2003, a closed season for all grouper was implemented from 
February 15 to March 15 in all waters of the Mexican Exclusive Economic 
Zone. Although aimed at protecting red grouper, E. morio, this closure 
protects Nassau grouper during a part of its spawning season (Aguilar-
Perera et al. 2008). A management plan was to have gone into effect in 
2012 to protect all commercially exploited groupers in Mexico's 
southern Gulf of Mexico and Caribbean Sea; the plan has not been 
    In the Turks and Caicos Islands, the only documented spawning 
aggregation site is protected from fishing in Northwest Point Marine 
National Park, Providenciales (DECR 2004; National Parks Ordinance and 
Subsidiary Legislation CAP. 80 of 1988). Similar to situations in other 
countries, full protection of Nassau grouper habitat as well as 
important spawning migration corridors on the very narrow fringe of 
Caicos Bank is problematic/yields unintended consequences. It would 
impose economic hardship on local fishers who depend on those areas for 
retrieving commercial species (e.g., spiny lobsters) and subsistence 
fishing (Rudd 2004).
    Take and possession of Nassau grouper have been prohibited since 
1990 in U.S. federal waters, including federal waters around Puerto 
Rico and the U.S.V.I. Since 1993, a ban on fishing/possessing Nassau 
grouper was implemented for the state of Florida and has been enacted 
in all U.S. state waters. The species was fully protected in both state 
and federal waters in Puerto Rico by 2004. The Caribbean Fishery 
Management Council, with support of local fishermen, established a no-
take marine protected area off the southwest coast of St. Thomas, 
U.S.V.I. in 1990. This area, known as the Hind Bank Marine Conservation 
District (HBMCD) (Brown 2007), was intended to protect red hind and 
their spawning aggregations, as well as a former Nassau grouper 
spawning site. The HBMCD was first subject to a seasonal closure, 
beginning in 1990 (Beets and Friedlander 1999, Nemeth 2005, Nemeth et 
al. 2006) to protect spawning aggregations of red hind, and was later 
closed to fishing year-round in 1998 (DPNR 2005). Additional fishing 
restrictions in the U.S.V.I. such as gear restrictions, rules on the 
sale of fish, and protected areas such as the Virgin Islands Coral Reef 
National Monument and Buck Island Reef National Monument where all take 
is prohibited, Virgin Islands National Park (commercial fishing 
prohibited), and several U.S.V.I. marine reserves offer additional 
protection to Nassau grouper. In 2006, the U.S.V.I. instituted 
regulations to prohibit Harvest and possession of Nassau grouper in 
territorial waters and fileting at sea was

[[Page 51938]]

prohibited (Garc[iacute]a-Moliner and Sadovy 2007).
    We are not aware of special conservation or management regulations 
for Nassau grouper in Anguilla. In Antigua-Barbuda, while Nassau 
grouper is not specifically managed or protected, closed seasons were 
considered in 2008 for Nassau grouper and red hind, the status of these 
closed seasons is not known. In the British Virgin Islands, there is a 
closed season for landing Nassau grouper between March 1 and May 31 
(Munro and Blok 2005). In Colombia, the San Andr[eacute]s Archipelago 
has a number of areas that are designated as no-take fishing zones, and 
in 2000 the entire archipelago was declared by UNESCO as the Seaflower 
Biosphere Reserve. In 2004, large portions of the archipelago were 
declared as a system of marine protected areas with varying zones of 
fisheries management; however, enforcement is largely lacking (M. 
Prada, Coralina, San Andres, Colombia, pers. comm. R. Hill, NMFS, 
2010). Right-to-fish laws in Colombia also require that fishermen be 
allowed to fish at a subsistence level even within the no-take zones 
(M. Prada, Coralina, San Andres, Colombia, pers. comm. R. Hill, NMFS, 
    The catch and sale of ripe female Nassau grouper during the 
spawning season is not allowed in the Dominican Republic (Bohnsack 
1989, Sadovy and Eklund 1999, Box and Bonilla Mejia 2008) and at least 
one marine park has been established with fishing regulations. In 
Guadeloupe and Martinique, there are plans to protect the species (F. 
Gourdin, Regional Activity Center for Specially Protected Areas and 
Wildlife--UNEP, pers. comm. to Y. Sadovy, University of Hong Kong, 
2011) although no details are available at this time. There is no 
legislation that controls fishing in the snapper/grouper fishery in 
Honduras although traps and spear are illegal in the Bay Islands. There 
are no special regulations for Nassau grouper in Jamaica specifically; 
however, some marine protected areas were designated in 2011.

Conclusions and Effectiveness Regarding Inadequacy of Existing 
Regulatory Mechanisms

    Overall, existing regulatory mechanisms throughout the species' 
range vary in effectiveness in addressing the most serious threat to 
Nassau grouper, fishing of spawning aggregations. In some countries, an 
array of national regulatory mechanisms, increase in MPAs, and 
customary management may be effective at addressing fishing of spawning 
aggregations. For example, the Exuma Cays Land and Sea Park (Bahamas), 
has been closed to fishing for over 25 years and protects both nursery 
and adult habitat for Nassau grouper and other marine species, such as 
queen conch, spiny lobster and marine turtles. There is a clear 
difference in the number, biomass, and size of all large grouper 
species between fished and non-fished areas (Sluka et al. 1996).
    We note, however, that many relevant countries have few, if any, 
Nassau grouper-specific regulations. Instead they rely on general 
fisheries regulations (e.g., Anguilla, Antigua-Barbuda, Colombia, and 
Cuba all rely on size limits as their only regulations and they are 
inadequate, while Guadeloupe and Martinique, Honduras, Jamaica, Mexico, 
St. Lucia, and the Turks and Caicos rely on a variety of general 
fishing regulations). Additionally, where regulations do exist, the 
ERAG indicated that law enforcement was insufficient, thus rendering 
the regulations ineffective.
    Further, the regulations may be ephemeral, unprotective of 
migrating adults, or inadequate to conserve the biological status of a 
species. For example, the Bahamas closed season is reconsidered 
annually and sometimes not implemented (we are aware of only one year 
the closed season has not been implemented, 2008). Regulations also do 
not protect all the known spawning aggregations (e.g., Belize, where 2 
spawning aggregations are fished by license). No protections were found 
in any country for the species as they migrate to and from the spawning 
aggregation sites. There are exemptions for ``historical,'' ``local,'' 
or artisanal fishermen (e.g., Colombia). Finally, there are other 
regulations that are insufficient to protect the species (e.g., size 
limit in the Bahamas is 3 cm shorter than the size-at-maturity, in Cuba 
it is 16 cm shorter than size-at-maturity).
    In some places (e.g., Bermuda), no recovery has been documented 
after 20 years of regulations (B. Luckhurst, Bermuda Department of 
Agriculture, Fisheries, and Parks, pers. comm. to Y. Sadovy, University 
of Hong Kong, September, 2012). In other places (e.g. Cayman Islands) 
there are indications of recovery at spawning aggregation sites, but 
fishing continues to keep the population depressed (Semmens et al. 
2012). Additionally, larval recruitment is highly variable due to 
currents in the Caribbean basin. Some populations may receive larval 
input from neighboring spawning aggregations, while local circulation 
patterns may entrain larvae (Colin et al. 1987) making the population 
entirely self-recruiting.
    In conclusion, the trends in the number and size of spawning 
aggregations indicate inadequate existing regulatory mechanisms and a 
lack of law enforcement leading to an increased risk of extinction for 
Nassau grouper.

E. Other Natural or Manmade Factors Affecting Its Continued Existence

    We considered climate change threats to Nassau grouper including 
global warming, sea level rise, and ocean acidification for Factor E. 
Although Nassau grouper occur across a range of temperatures, spawning 
occurs when sea surface temperatures range between 25 [deg]C-26 [deg]C. 
Because Nassau grouper only spawn in a very narrow window of 
temperatures, a rise in sea surface temperature above the correct range 
could cause spawning to cease or force the species to shift its 
geographic range to find the correct temperature range. A potential 
effect of climate change could also be the loss of structural habitat 
in the coral reef ecosystems where ocean acidification is anticipated 
to affect the integrity of coral reefs (Munday et al. 2008). If sea 
level changed rapidly, coral reef depth regime may be modified with 
such rapidity that coral and coral reefs will be affected (Munday et 
al. 2008). Increased sea surface temperatures have been responsible for 
coral loss through bleaching and disease. Bioerosion may reduce 3-
dimensional structure in affected areas (Alvarez-Filip et al. 2009), 
reducing adult habitat for Nassau grouper (Coleman and Koenig 2010, 
Rogers and Beets 2001). Increased global temperatures are also 
predicted to change parasite-host relationships and may present unknown 
concerns (Harvell et al. 2002, Marcogliese 2001). The ERAG ranking 
indicated that climate change was an ``unknown risk'' to Nassau 
    We also considered threats from aquaculture to Nassau grouper under 
Factor E. Experiments to determine the success rate of larval Nassau 
grouper culture (Watanabe et al. 1995a, 1995b) and survival of released 
hatchery-reared juveniles (Roberts et al. 1994) have been conducted and 
feasibility of restocking reefs has been tested (Roberts et al. 1995) 
in St. Thomas, U.S.V.I. The potential of Nassau grouper stock 
enhancement, as with any other grouper species, has yet to be 
determined (Roberts et al. 1995). Serious concerns about the genetic 
consequences of introductions and about possible problems of juvenile 
habitat availability, introduction of maladapted individuals, or 
inability to locate traditional spawning aggregations, continue to be 
raised. The ERAG ranking indicated that

[[Page 51939]]

aquaculture was a ``very low risk'' to Nassau grouper.
    The demographic factors of growth rate/productivity and diversity 
were also considered under Factor E. To assess these demographic 
factors, ERAG members considered whether the species' average 
population growth rate is likely to be above the population loss 
(either natural or anthropogenic) such that an appropriate abundance is 
maintained. They also considered whether the species is at risk due to 
a loss in the breeding population, which leads to a reduction in 
survival and production of eggs and offspring. The ERAG also considered 
whether the species exhibits trends or shifts in demographic or 
reproductive traits that point to a decline in population growth rate. 
The ERAG ranking indicated that growth rate/productivity of Nassau 
grouper was an ``increasing risk'' for the species and that diversity 
was a ``moderate risk.'' We agree with these rankings and believe they 
are supported by the declining number and size of spawning 
aggregations, which affects growth rate/productivity and diversity.

Protective Efforts

    Section 4(b)(1)(A) of the ESA requires the Secretary, when making a 
listing determination for a species, to take into consideration those 
efforts, if any, being made by any State or foreign nation to protect 
the species. In judging the efficacy of not yet implemented efforts or 
efforts that have been implemented, but have not yet demonstrated 
whether they are effective, we rely on the Services' joint ``Policy for 
Evaluation of Conservation Efforts When Making Listing Decisions'' 
(``PECE''; 68 FR 15100; March 28, 2003). The PECE is designed to ensure 
consistent and adequate evaluation on whether any conservation efforts 
that have been recently adopted or implemented, but not yet proven to 
be successful, will result in recovering the species to the point at 
which listing is not warranted or contribute to forming the basis for 
listing a species as threatened rather than endangered. The PECE is 
expected to facilitate the development of conservation efforts by 
states and other entities that sufficiently improve a species' status 
so as to make listing the species as threatened or endangered 
    The PECE establishes two basic criteria to use in evaluating 
efforts identified in conservations plans, conservation agreements, 
management plans or similar documents: (1) the certainty that the 
conservation efforts will be implemented; and (2) the certainty that 
the efforts will be effective. We evaluated conservation efforts to 
protect and recover Nassau grouper that are either underway but not yet 
fully implemented, or are only planned.
    Conservation efforts with the potential to address threats to 
Nassau grouper include, but are not limited to fisheries management 
plans, education about overfishing and fishing of spawning 
aggregations, and projects addressing the health of coral reef 
ecosystems. These conservation efforts may be conducted by countries, 
states, local governments, individuals, NGOs, academic institutions, 
private companies, individuals, or other entities. They also include 
global conservation organizations that conduct coral reef and/or marine 
environment conservation projects, global coral reef monitoring 
networks and research projects, regional or global conventions, and 
education and outreach projects throughout the range of Nassau grouper. 
The Biological Report summarizes all known conservation efforts, 
including those that have yet to be fully implemented or have yet to 
demonstrate effectiveness. Conservation efforts that have yet to be 
fully implemented included Mexico's 2012 proposed management plan, 
Antigua-Barbuda's 2008 closed season proposal, and Guadeloupe and 
Martinique's plans to protect the species. Because these proposed plans 
are two to six years old with no updates or known implementation, we 
find that they fail to meet the PECE criterion regarding certainty of 
implementation. Based on Jamaica's historic overfishing and difficulty 
in enforcing existing regulations, we find that the marine protected 
areas implemented in 2011 fail to meet the second PECE criterion 
regarding certainty of effectiveness. All other known conservation 
efforts have been implemented for extended periods of time and have 
failed to satisfy the criteria of the PECE as evidenced by the 
continued decline in size and number of spawning aggregations. After 
taking into account these conservation efforts, our evaluation of the 
section 4(a)(1) factors is that the conservation efforts identified 
cannot be considered effective measures in reducing the current 
extinction risk.

Significant Portion of Range

    There are two situations under which a species is eligible for 
listing under ESA: a species may be endangered or threatened throughout 
all of its range or a species may be endangered or threatened 
throughout only a ``significant portion of its range'' (SPOIR). 
Although the ESA does not define ``SPOIR,'' NMFS and the U.S. Fish and 
Wildlife Service (USFWS) published a final policy clarifying their 
interpretation of this phrase (79 FR 37577; July 7, 2014). Under the 
policy, if a species is found to be endangered or threatened throughout 
only a significant portion of its range, the entire species is subject 
to listing and must be protected everywhere. A portion of a species' 
range is ``significant'' if ``. . . the species is not currently 
endangered or threatened throughout its range, but the portion's 
contribution to the viability of the species is so important that, 
without the members in that portion, the species would be in danger of 
extinction, or likely to become so in the foreseeable future, 
throughout all of its range.'' Thus, if the species is found to be 
threatened or endangered throughout its range, we do not separately 
evaluate portions of the species' range.
    Although the SPOIR Policy had yet to go into effect during our 
status review of Nassau grouper, we considered the interpretations and 
principles contained in the Draft Policy with regards to the Nassau 
grouper and completed and assessment of potential ``SPOIR,'' which is 
documented in the ERAG responses. However, given our conclusion that 
the Nassau grouper is threatened throughout its range, under our final 
policy, there is no portion of the range that can be considered 

Results of Extinction Risk Analysis

    Based on the rankings by the ERAG, the greatest threats to Nassau 
grouper are historical harvest, inadequate law enforcement, and fishing 
of spawning aggregations, all of which were ranked as are ``high risk'' 
threats. Growth rate/productivity, spatial structure/connectivity, and 
foreign regulations were rated as ``increasing risks,'' meaning they 
are likely to be posing only low to moderate risk to the species now 
but are expected to pose a high risk in the foreseeable future. 
Abundance, diversity, commercial harvest, artificial selection, and 
state and territory regulations, were rates as ``moderate risks,'' and 
thus may not contribute significantly to the extinction risk of the 
species now but are likely pose long term risks to the species. Habitat 
alteration, aquaculture, U.S. federal regulations, disease, parasites, 
and abnormalities were rated as ``very low'' to ``low'' risks and thus 
are unlikely to be affecting the species extinction risk or status.
    We concur with these overall results and conclude that the ``high 
risk'' threats are driving the extinction risk for Nassau grouper. 
Based on the information in the Biological Report and

[[Page 51940]]

the results from the ERAG, we conclude that the ESA Factor D, 
inadequacy of regulatory mechanisms, particularly in regards to fishing 
spawning aggregations, is contributing to an increased risk of 
extinction for Nassau grouper. Fishing on spawning aggregations and 
lack of regulatory control and law enforcement greatly reduce 
reproductive output, which reduces recruitment. If growth and sexual 
recruitment rates cannot balance the loss from mortality, populations 
become more vulnerable to extinction (Primack 1993).

Key Conclusions From Biological Review

    The species is made up of a single population over its entire 
geographic range. As discussed in detail in the Biological Report and 
summarized above, there is no evidence to suggest the existence of 
genetic differences between Nassau grouper in different portions of the 
range. Multiple genetic analyses indicate that there is high gene flow 
throughout the geographic range of the Nassau grouper, and no clearly 
defined population substructuring has been observed. Accordingly, we 
conclude that the species is comprised of a single panmictic 
    The species has patchy abundance, being depleted or absent in many 
areas. This conclusion is based on the Biological Report, which 
describes the reduction in size and number of spawning aggregations 
throughout the range. Patchy abundance throughout the range of a 
species is common and due to differences in habitat quality/quantity or 
exploitation levels at different locations. However, for Nassau 
grouper, dramatic, consistent declines have been noted throughout the 
species range. In many areas throughout the Caribbean, the species is 
now commercially extinct or spawning aggregations have been extirpated 
with no signs of recovery.
    The species possesses life history characteristics that increase 
vulnerability to harvest, including slow growth with late maturation, 
large size, formation of large spawning aggregations, and occur in 
shallow habitat. This conclusion is based on the Description of the 
Species in the Biological Report (Hill and Sadovy de Mitcheson 2013). 
Slow growth leading to late maturation exposes sub-adults to harvest 
prior to reproduction. Sub-adult and adult Nassau grouper form large 
conspicuous spawning aggregations. These aggregations are often in 
shallow habitat areas that are easily accessible to fishermen and are 
heavily exploited. There are existing spawning aggregations, that while 
reduced in size and number, still function and provide recruits to the 
    The species is broadly distributed, and its current range is 
similar to its historical range. This conclusion is based on the Range 
Wide Distribution section of the Biological Report (Hill and Sadovy de 
Mitcheson 2013), which concluded that available information suggests 
that the current range is equivalent to the historical range though 
abundance has been severely depleted.

Key Conclusions From Threats Evaluation

    The three most important threats to Nassau grouper are spawning 
aggregation fishing, historical harvest, and lack of law enforcement. 
These three threats were rated as ``high risk'' threats to the species 
by the ERAG. Growth rate/productivity, spatial structure/connectivity, 
and foreign regulations are ``increasing risks.'' Abundance, diversity, 
commercial harvest, artificial selection, and state and territory 
regulations are ``moderate risks.'' Habitat alteration, aquaculture, 
U.S. federal regulations, and disease, parasites, and abnormalities are 
``very low'' to ``low'' risk.
    Existing regulatory mechanisms are insufficient in addressing the 
most serious threat to Nassau grouper. As discussed above in the 
``Overall Conclusions Regarding Inadequacy of Existing Regulatory 
Mechanisms,'' national and/or local laws and regulations are not 
addressing the most important threat, fishing spawning aggregations, to 
an acceptable extent. Because of the inadequacy of regulatory 
mechanisms (Factor D), Nassau grouper are at an increased risk of 


    Based on the key conclusions from the Biological Report and the 
Extinction Risk Analysis, we summarize the results of our comprehensive 
status review as follows: (1) The species is made up of a single 
population over a broad geographic range, and its current range is 
indistinguishable from its historical range; (2) the species possesses 
life history characteristics that increase vulnerability to harvest; 
(3) spawning aggregations are declining in size and number across the 
species' range; (4) existing regulatory mechanisms and a lack of law 
enforcement throughout the species' range are not effective in 
addressing fishing spawning aggregations; and (5) the combination of 
life history characteristics and existing regulatory mechanisms 
indicate that the species is not currently in danger of extinction, but 
it is likely to become in danger of extinction in the foreseeable 
    Based on these results, we conclude that the Nassau grouper is not 
currently in danger of extinction throughout its range, but is likely 
to become in danger of extinction throughout its range within the 
foreseeable future. Accordingly, we find that the species meets the 
definition of threatened and propose to list it as threatened under the 

Effects of Listing

    Conservation measures provided for species listed as endangered or 
threatened under the ESA include recovery plans (16 U.S.C. 1553(f)), 
critical habitat designations, Federal agency consultation requirements 
(16 U.S.C. 1536), and prohibitions on taking (16 U.S.C. 1538). 
Recognition of the species' status through listing promotes 
conservation actions by Federal and state agencies, private groups, and 
individuals, as well as the international community. Should the 
proposed listing be made final, a recovery program could be 
implemented, and critical habitat will be designated to the maximum 
extent prudent and determinable. We anticipate that protective 
regulations for Nassau grouper may need to be developed in the context 
of conserving aquatic ecosystem health. Federal, state, and the private 
sectors will need to cooperate to conserve listed Nassau grouper and 
the ecosystems upon which they depend.

Identifying ESA Section 7 Consultation Requirements

    Section 7(a)(4) of the ESA and NMFS/USFWS regulations require 
Federal agencies to confer with us on actions likely to jeopardize the 
continued existence of species proposed for listing, or likely to 
result in the destruction or adverse modification of proposed critical 
habitat. If a proposed species is ultimately listed, Federal agencies 
must consult under section 7 on any action they authorize, fund, or 
carry out if those actions may affect the listed species or designated 
critical habitat. Based on currently available information, we can 
conclude that examples of Federal actions that may affect Nassau 
grouper include, but are not limited to: artificial reef creation, 
dredging, pile-driving, military activities, and fisheries management 

Critical Habitat

    Critical habitat is defined in section 3 of the ESA (16 U.S.C. 
1532(5)) as: (1) the specific areas within the geographical area 
occupied by a species, at the time

[[Page 51941]]

it is listed in accordance with the ESA, on which are found those 
physical or biological features (a) essential to the conservation of 
the species and (b) that may require special management considerations 
or protection; and (2) specific areas outside the geographical area 
occupied by a species at the time it is listed upon a determination 
that such areas are essential for the conservation of the species. 
``Conservation'' means the use of all methods and procedures needed to 
bring the species to the point at which listing under the ESA is no 
longer necessary. Regulations require that we shall designate critical 
habitat in areas outside the geographical area presently occupied by a 
species only when a designation limited to its present range would be 
inadequate to ensure the conservation of the species (50 CFR 424.12 
(e)). Critical habitat cannot be designated within foreign countries or 
in other areas outside of United States jurisdiction (50 CFR 
    Section 4(a)(3)(A) of the ESA (16 U.S.C. 1533(a)(3)(A)) requires 
that, to the extent prudent and determinable, critical habitat be 
designated concurrently with the listing of a species. To the maximum 
extent prudent and determinable, we will publish a proposed designation 
of critical habitat for Nassau grouper in a separate rule. Designations 
of critical habitat must be based on the best scientific data available 
and must take into consideration the economic, national security, and 
other relevant impacts of specifying any particular area as critical 
habitat. Once critical habitat is designated, section 7 of the ESA 
requires Federal agencies to ensure that they do not fund, authorize, 
or carry out any actions that are likely to destroy or adversely modify 
that habitat. This requirement is in addition to the section 7 
requirement that Federal agencies ensure that their actions do not 
jeopardize the continued existence of listed species.

Identification of Those Activities That Would Constitute a Violation of 
Section 9 of the ESA

    Because we are proposing to list Nassau grouper as threatened, the 
ESA section 9 prohibitions do not automatically apply. Therefore, 
pursuant to ESA section 4(d), we will evaluate whether there are 
protective regulations we deem necessary and advisable for the 
conservation of Nassau grouper, including application of some or all of 
the take prohibitions. If protective regulations are deemed necessary, 
a proposed 4(d) rule would be subject to public comment.

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 (Public Law 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 
Biological Report. Five independent specialists were selected from the 
academic and scientific community, Federal and state agencies, and the 
private sector for this review (with three respondents). All peer 
reviewer comments were addressed prior to dissemination of the final 
Biological Report and publication of this proposed rule.


    A complete list of the references used in this proposed rule is 
available upon request (see ADDRESSES).


National Environmental Policy Act

    The 1982 amendments to the ESA, in section 4(b)(1)(A), restrict the 
information that may be considered when assessing species for listing. 
Based on this limitation of criteria for a listing decision and the 
opinion in Pacific Legal Foundation v. Andrus, 675 F. 2d 825 (6th Cir. 
1981), NMFS has concluded that ESA listing actions are not subject to 
the environmental assessment requirements of the National Environmental 
Policy Act (See NOAA Administrative Order 216-6).

Executive Order 12866, Regulatory Flexibility Act and Paperwork 
Reduction Act

    As noted in the Conference Report on the 1982 amendments to the 
ESA, economic impacts cannot be considered when assessing the status of 
a species. Therefore, the economic analysis requirements of the 
Regulatory Flexibility Act are not applicable to the listing process. 
In addition, this proposed rule is exempt from review under Executive 
Order 12866. This proposed rule does not contain a collection-of-
information requirement for the purposes of the Paperwork Reduction 


    In keeping with the intent of the Administration and Congress to 
provide continuing and meaningful dialogue on issues of mutual state 
and Federal interest, this proposed rule will be given to the relevant 
governmental agencies in the countries in which the species occurs, and 
they will be invited to comment. NMFS will confer with U.S. Department 
of State to ensure appropriate notice is given to foreign nations 
within the range of the species. As the process continues, NMFS intends 
to continue engaging in informal and formal contacts with the U.S. 
State Department, giving careful consideration to all written and oral 
comments received.

Public Comments Solicited

    NMFS intends that any final action resulting from this proposal 
will be as accurate as possible and informed by the best available 
scientific and commercial information. Therefore, NMFS request comments 
or information from the public, other concerned governmental agencies, 
the scientific community, industry, or any other interested party 
concerning this proposed rule. NMFS particularly seek comments 
    (1) Information concerning the location(s) and status of any 
spawning aggregations of the species; and
    (2) Information concerning the threats to the species; and
    (3) Efforts being made to protect the species throughout its 
current range.

Public hearing requests must be requested by October 17, 2014.

List of Subjects in 50 CFR Part 224

    Administrative practice and procedure, Endangered and threatened 
species, Exports, Imports, Reporting and recordkeeping requirements, 

    Dated: August 22, 2014.
Samuel D. Rauch III,
Deputy Assistant Administrator for Regulatory Programs, National Marine 
Fisheries Service.

    For the reasons set out in the preamble, we propose to amend 50 CFR 
Chapter II part 223 as follows:


1. The authority citation for part 223 continues to read as follows:

    Authority: 16 U.S.C. 1531-1543; subpart B, Sec.  223.201-202 
also issued under 16 U.S.C. 1361 et seq.; 16 U.S.C. 5503(d) for 
Sec.  223.206(d)(9).

[[Page 51942]]

2. In Sec.  223.102, amend the table in paragraph (e) by adding new 
entry ``Grouper, Nassau'' in alphabetical order under the ``Fishes'' 
table subheading to read as follows:

Sec.  223.102  Enumeration of threatened marine and anadromous species.

* * * * *
    (e) The threatened species under the jurisdiction of the Secretary 
of Commerce are:

                           Species \1\
------------------------------------------------------------------  Citation(s) for     Critical
                                                  Description of        listing          habitat      ESA rules
         Common name            Scientific name    listed entity    determination(s)
                                                  * * * * * * *
                                                  * * * * * * *
Grouper, Nassau..............  Epinephelus       Entire species..  [Insert Federal             NA            NA
                                striatus.                           Register
                                                                    citation and
                                                                    date when
                                                                    published as a
                                                                    final rule].
                                                  * * * * * * *
\1\ Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement,
  see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56
  FR 58612, November 20, 1991).

* * * * *
[FR Doc. 2014-20811 Filed 8-29-14; 8:45 am]