81_FR_42393 81 FR 42268 - Endangered and Threatened Wildlife and Plants: Final Listing Determination on the Proposal To List the Nassau Grouper as Threatened Under the Endangered Species Act

81 FR 42268 - Endangered and Threatened Wildlife and Plants: Final Listing Determination on the Proposal To List the Nassau Grouper as Threatened Under the Endangered Species Act

DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration

Federal Register Volume 81, Issue 125 (June 29, 2016)

Page Range42268-42285
FR Document2016-15101

We, NMFS, are publishing this final rule to implement our determination to list the Nassau grouper (Epinephelus striatus) as threatened under the Endangered Species Act of 1973, as amended (ESA). We have completed a status review of the Nassau grouper in response to a petition submitted by WildEarth Guardians. After reviewing the best scientific and commercial data available, including the status review and comments received on the proposed rule, we have determined that the Nassau grouper meets the definition of a threatened species. While the species still occupies its historical range, overutilization through historical harvest has reduced the number of individuals which in turn has reduced the number and size of spawning aggregations. Although harvest of Nassau grouper has diminished due to management measures, the reduced number and size of spawning aggregations and the inadequacy of law enforcement continue to present extinction risk to Nassau grouper. Based on these considerations, described in more detail within this action, 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 also solicit information that may be relevant to the designation of critical habitat for Nassau grouper, including information on physical or biological features essential to the species' conservation, areas containing these features, and potential impacts of a designation.

Federal Register, Volume 81 Issue 125 (Wednesday, June 29, 2016)
[Federal Register Volume 81, Number 125 (Wednesday, June 29, 2016)]
[Rules and Regulations]
[Pages 42268-42285]
From the Federal Register Online  [www.thefederalregister.org]
[FR Doc No: 2016-15101]


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DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

50 CFR Part 223

[Docket No. 1206013326-6497-03]
RIN 0648-XA984


Endangered and Threatened Wildlife and Plants: Final Listing 
Determination on the Proposal To List the Nassau Grouper as Threatened 
Under the Endangered Species Act

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

ACTION: Final rule; request for information.

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SUMMARY: We, NMFS, are publishing this final rule to implement our 
determination to list the Nassau grouper (Epinephelus striatus) as 
threatened under the Endangered Species Act of 1973, as amended (ESA). 
We have completed a status review of the Nassau grouper in response to 
a petition submitted by WildEarth Guardians. After reviewing the best 
scientific and commercial data available, including the status review 
and comments received on the proposed rule, we have determined that the 
Nassau grouper

[[Page 42269]]

meets the definition of a threatened species. While the species still 
occupies its historical range, overutilization through historical 
harvest has reduced the number of individuals which in turn has reduced 
the number and size of spawning aggregations. Although harvest of 
Nassau grouper has diminished due to management measures, the reduced 
number and size of spawning aggregations and the inadequacy of law 
enforcement continue to present extinction risk to Nassau grouper. 
Based on these considerations, described in more detail within this 
action, 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 also solicit 
information that may be relevant to the designation of critical habitat 
for Nassau grouper, including information on physical or biological 
features essential to the species' conservation, areas containing these 
features, and potential impacts of a designation.

DATES: The effective date of this final rule is July 29, 2016. 
Information on features, areas, and potential impacts, that may support 
designation of critical habitat for Nassau grouper must be received by 
August 29, 2016.

ADDRESSES: Information regarding this final rule may be obtained by 
contacting NMFS, Southeast Regional Office, 263 13th Avenue South, 
Saint Petersburg, FL 33701. Supporting information, including the 
Biological Report, is available electronically on the NMFS Web site at: 
http://sero.nmfs.noaa.gov/protected_resources/listing_petitions/species_esa_consideration/index.html.
    You may submit information regarding potential critical habitat 
designation to the Protected Resources Division by either of the 
following methods:
     Electronic Submissions: Submit all electronic comments via 
the Federal eRulemaking Portal. Go to www.regulations.gov/#!docketDetail;D=NOAA-NMFS-2015-0130, click the ``Comment Now!'' icon, 
complete the required fields, and enter or attach your comments.
     Mail: Submit written information to the Protected 
Resources Division, NMFS Southeast Regional Office, 263 13th Avenue 
South, Saint Petersburg, FL 33701.

FOR FURTHER INFORMATION CONTACT: Adam Brame, NMFS, Southeast Regional 
Office (727) 209-5958; or Lisa Manning, NMFS, Office of Protected 
Resources (301) 427-8466.

SUPPLEMENTARY INFORMATION: 

Background

    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. The petition asserted that (1) the present or 
threatened destruction, modification, or curtailment of habitat or 
range; (2) overutilization for commercial, recreational, scientific, or 
educational purposes; (3) inadequacy of existing regulatory mechanisms; 
and (4) other natural or manmade factors are affecting the continued 
existence of and contributing to the imperiled statuses of these 
species. The petitioner also requested that critical habitat be 
designated for these species concurrent with listing 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 (76 FR 31592, June 1, 2011; 77 FR 
25687, May 1, 2012; 77 FR 61559, October 10, 2012).
    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). At that time, we announced the 
initiation of a formal status review and requested scientific and 
commercial information from the public on: (1) The 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.
    As part of the status review process to determine whether the 
Nassau grouper warrants listing under the ESA, we completed a 
Biological Report and an extinction risk analysis (ERA). The Biological 
Report summarizes the taxonomy, distribution, abundance, life history, 
and biology of the species. 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. We used the 
Biological Report to complete a threats evaluation and an ERA to 
determine the status of the species.
    After completing the Biological Report and considering the 
information received on the 90-day finding, we published a proposed 
rule to list Nassau grouper as a threatened species on September 2, 
2014 (79 FR 51929). During a 90-day comment period, we solicited 
comments on our proposal from the public and any other interested 
parties.

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.''
    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 in danger 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).
    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

[[Page 42270]]

existing regulatory mechanisms; or (E) other natural or manmade factors 
affecting its continued existence (sections 4(a)(1)(A) through (E)). We 
are required 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.
    In determining whether the Nassau grouper meets the standard of 
endangered or threatened, we followed a stepwise approach. First we 
considered the specific life history, ecology, and status of the 
species as documented in the Biological Report. We then considered 
information on factors adversely affecting and posing extinction risk 
to the species in a threats evaluation. In this evaluation we assessed 
the threats affecting the status of the species using the factors 
identified in ESA section 4(a)(1). We considered the nature of the 
threats and the species response to those threats. We also considered 
each threat identified, both individually and cumulatively. Once we 
evaluated the threats, we assessed the efforts being made to protect 
the species to determine if these conservation efforts were adequate to 
mitigate the existing threats and alter extinction risk. Finally, we 
considered the public comments received in response to the proposed 
rule. In making this finding, we have relied on the best available 
scientific and commercial data.

Summary of Comments Received

    Below we address the comments received on the proposed listing for 
Nassau grouper. In response to our request for public comments, we 
received 17 written responses. The overall feedback was supportive of 
the rule with the exception of three commenters, who believe current 
regulations within the United States are sufficient in protecting this 
species. No comments addressed threats to Nassau grouper throughout the 
rest of their range. We did not receive any information on additional 
conservation efforts being taken.
    Comment 1: Multiple commenters supported the proposed rule to list 
Nassau grouper as a threatened species and further encouraged regional 
collaboration to develop adequate management measures.
    Response: We agree that regional collaboration will strengthen 
efforts to consistently manage and conserve the species, and we hope 
this listing will encourage collaborative efforts. In some cases, 
adding a species to the endangered species list leads to increased 
funding opportunities and potential for collaboration between state and 
federal partners, as well as stakeholders. We will seek regional 
collaborative conservation efforts within the Caribbean region to 
further the conservation of the species.
    Comment 2: We received comments that the existing management 
measures implemented by Fishery Management Councils are already 
effective at protecting Nassau grouper within U.S. waters, (including 
U.S. territorial waters of Puerto Rico and the U.S. Virgin Islands) and 
that the listing may add unnecessary burdens on our domestic fisheries.
    Response: We agree that the South Atlantic Fishery Management 
Council and the Caribbean Fishery Management Council have taken 
significant steps to protect and rebuild the Nassau grouper population 
in U.S. waters. Unfortunately, a large part of the species' range and 
population is outside of U.S. jurisdiction and is therefore not 
directly aided by Council protections. We must make our determination 
based on the best scientific and commercial data available, independent 
of the potential burdens to our other domestic fisheries. This standard 
has been applied when making the Nassau grouper final listing 
determination.
    Comment 3: Some comments expressed concern over the economic 
consequences of listing Nassau grouper, including possible effects on 
commercial fishermen.
    Response: We are unable to consider economic impacts in a listing 
determination. The ESA requires us to make listing determinations by 
evaluating the standards and factors in section 4 of the ESA, and based 
solely on the best scientific and commercial data available. Listing 
Nassau grouper as a threatened species would not create any immediate 
additional regulatory requirements directly affecting commercial 
fishermen. Potential future regulations affecting conservation of 
Nassau grouper, including take and import regulations may be proposed 
via a separate rulemaking process which would include consideration of 
certain economic impacts (e.g., impacts on small businesses) and 
opportunities for public input. Individuals that require federal 
permits or funding for actions that might affect Nassau grouper might 
need to make adjustments to their activities to avoid jeopardizing 
Nassau grouper, and to avoid or minimize take of the species, but that 
would be a determination for a specific section 7 consultation in the 
future.
    Comment 4: Several comments indicated that spawning aggregation 
sites need to be protected and that proper enforcement of both existing 
and future rules is paramount in protecting the species.
    Response: We agree that the lack of adequate protections for Nassau 
grouper spawning aggregations and the inadequacy of law enforcement are 
major contributors to the species' decline throughout its range. These 
threats were rated `high' during the ERA as explained in the proposed 
rule and, as such, were taken into consideration when making our final 
listing determination.
    Comment 5: One commenter supported the rule stating, ``We agree 
that the best available science demonstrates that Nassau grouper is 
likely to be at risk of extinction in the foreseeable future, and may 
in fact be in danger of extinction now.'' They further encouraged swift 
designation of critical habitat to protect spawning aggregation sites, 
nursery and juvenile habitat, and feeding habitat.
    Response: We acknowledge the concern raised by the commenter that 
the species may be in danger of extinction now and provide further 
detail below as to how we reached our listing determination in this 
final rule. With regard to critical habitat, section 4(a)(3)(A) of the 
ESA (16 U.S.C. 1533(a)(3)(A)) requires that, if prudent and 
determinable, critical habitat be designated concurrently with the 
listing of a species. We do not currently have sufficient information 
to determine what physical and biological features within Nassau 
grouper habitats facilitate the species' life history strategy and thus 
are essential to the species' conservation. Therefore, we cannot yet 
determine what areas meet the definition of critical habitat under the 
ESA. Because critical habitat is not currently determinable, we will 
not designate critical habitat concurrently with this final rule. 
Designation of critical habitat may occur via a subsequent rule-making 
process if we can identify critical habitat and designation is prudent. 
We are soliciting information on features, areas, and impacts of 
designation, that may support designation of critical habitat for 
Nassau grouper.
    Comment 6: One commenter suggested the use of size restrictions, 
monitoring, closed fishing seasons for the protection of spawning 
aggregations, and the use of marine protected areas as measures to 
protect the species.
    Response: We summarize in this rule the existing regulations 
currently in place throughout the Caribbean Sea that

[[Page 42271]]

include many of these suggested practices. Within U.S. waters, measures 
to protect Nassau grouper are already in place under the Magnuson-
Stevens Act and State and Territorial fishery management authorities. 
As a species listed as threatened under the ESA, any federal action 
implemented, authorized or funded that ``may affect'' Nassau grouper 
will require consultation to ensure the action is not likely to 
jeopardize the species' continued existence. We may also implement 
additional protective regulations for Nassau grouper under section 4(d) 
of the ESA if we determine such regulations are necessary and advisable 
for the conservation of this threatened species. Issuance of a 4(d) 
rule would be a separate rule-making process that would include 
specific opportunities for public input.
    Comment 7: The U.S. Navy identified three Navy installations or 
properties that are within the geographic range of Nassau grouper. They 
expressed concern over their ability to utilize and maintain those 
areas with a listing and designation of critical habitat. In 
particular, the Navy expressed concern over their ability to conduct 
maintenance dredging and requested we consult with them prior to 
proposing critical habitat.
    Response: A rule to list Nassau grouper will require federal 
agencies to assess whether any actions implemented, authorized, or 
funded within the range of the species ``may affect'' Nassau grouper, 
and consult with NMFS to ensure their actions are not likely to 
jeopardize the species' continued existence. The rule-making process 
for identifying critical habitat is separate from this final listing 
rule and would include opportunities for public participation and 
input, as well as coordination with all military branches. Unlike ESA 
listing decisions, the designation of critical habitat requires us to 
consider economic, national security, and other impacts of the 
designation.
    Comment 8: One commenter opposed the proposed rule to list Nassau 
grouper as a threatened species stating this is ``merely a precursor to 
an attempt to form a basis for a push for Marine Protection Areas.''
    Response: The proposed rule to list Nassau grouper was the result 
of the petition we received from WildEarth Guardians, our 90-day 
finding that the petition presented substantial information that 
listing may be warranted, and our 12-month finding that listing as a 
threatened species was warranted. 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. We have not 
proposed any additional regulations affecting management of Nassau 
grouper as a result of the proposed listing rule. However, we will need 
to determine whether we can identify critical habitat for this species, 
and if so, make an appropriate designation of critical habitat. A 
critical habitat designation could have implications for fishing 
activities. Any designation of critical habitat would include 
opportunities for public input. As previously mentioned, we could also 
implement additional protective regulations for Nassau grouper under 
section 4(d) of the ESA, if we determine they are necessary and 
advisable for the conservation of this threatened species. Issuance of 
a 4(d) rule would be a separate rule-making process that would include 
specific opportunities for public input.

Changes From the Proposed Rule

    In addition to responding to the comments, we made a number of 
changes in this final rule. These included making revisions to the 
Biological Review section (most notably in the Population Structure and 
Genetics, and the Fishing Impacts on Spawning Aggregations 
subsections), including a more detailed description of our role in the 
Threats Evaluation, providing more detail in the Extinction Risk 
Analysis section, and clarifying the role of foreign conservation 
measures as they relate to making our final listing determination. We 
made several of these changes to provide clarity on how we reached our 
listing determination in response to the comment that, ``. . . Nassau 
grouper is likely to be at risk of extinction in the foreseeable 
future, and may in fact be in danger of extinction now.''

Biological Review

    This section provides a summary of key biological information 
presented in the Biological Report (Hill and Sadovy de Mitcheson 2013), 
which provides the baseline context and foundation for our listing 
determination.

Species Description

    The Nassau grouper, E. striatus (Bloch 1792), is a long-lived, 
moderate sized serranid fish with large eyes and a robust body. 
Coloration is variable, but adult fish are generally buff, with five 
dark brown vertical bars, a large black saddle blotch on top of the 
base of the tail, and a row of black spots below and behind each eye. 
Color pattern can also 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 bicolor pattern is seen when two adults or 
an adult and large juvenile meet and is frequently observed at spawning 
aggregations (Heemstra and Randall 1993). There is also a distinctive 
dark tuning-fork mark that begins at the front of the upper jaw, 
extends back between the eyes, and then divides into two branches on 
top of the head behind the eyes. Another dark band runs from the tip of 
the snout through the eye and then curves upward to meet its 
corresponding band from the opposite side just in front of the dorsal 
fin. Juveniles exhibit a color pattern similar to adults (e.g., Silva 
Lee 1977).
    Maximum age has been estimated as 29 years, based on an ageing 
study using sagittal otoliths (Bush et al. 2006). Most studies indicate 
a rapid growth rate for juveniles, which has been estimated to be about 
10 mm/month total length (TL) for small juveniles, and 8.4 to 11.7 mm/
month TL for larger juveniles (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 interval between the birth of an individual 
and the subsequent birth of its first offspring) is estimated as 9-10 
years (Sadovy and Eklund 1999).

Distribution

    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 Nassau grouper 
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 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) in areas 
north of Key West or the Tortugas (Smith 1971). They are considered a 
rare or transient species off Texas in the northwestern Gulf of Mexico 
(Gunter and Knapp 1951 in Hoese and Moore 1998). The first confirmed 
sighting of Nassau grouper in the Flower Garden Banks National Marine 
Sanctuary, which is located in the northwest Gulf of Mexico

[[Page 42272]]

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 of their distribution.

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, juvenile Nassau grouper 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 rubble mounds, some from tilefish (Malacanthus 
plumieri), 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 (12-15 cm 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 (25-35 cm 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 shallower inshore waters (3.7-16.5 m) and larger individuals more 
common on deeper (18.3-54.9 m) 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 have larger 
home ranges with less overlap. Mean home range of adult Nassau grouper 
in the Bahamas was 18,305 m\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 
255 m (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 adult Nassau grouper as piscivorous (Randall and Brock 
1960, Randall 1965, Randall 1967, Carter et al. 1994, Eggleston et al. 
1998). Feeding can take place around the clock 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 standard length; SL) 
feed on a variety of plankton, including pteropods, amphipods, and 
copepods (Greenwood 1991, Grover et al. 1998).

Population Structure and Genetics

    Early genetic analyses indicated high gene flow throughout the 
geographic range of Nassau grouper but were unable to determine the 
relative contributions of populations (Hinegardner and Rosen 1972, 
Hateley 2005). A study of Nassau grouper genetic population structure, 
using mitochondrial DNA (mtDNA) and nuclear microsatellite DNA, 
revealed no clearly defined population substructuring based on samples 
from Belize, Cuba, Bahamas, and Florida. These data indicated that 
spawning aggregations are not exclusively self-recruiting and that 
larvae can disperse over great distances, but the relative importance 
of self-recruitment and larval immigration to local populations was 
unclear (Sedberry et al. 1996). Similarly, a study by Hateley (2005) 
that analyzed samples from Belize, Bahamas, Turks and Caicos, and 
Cayman Islands using enzyme electrophoresis indicated low to 
intermediate levels of genetic variability. Results from this study 
provided no evidence for population substructuring by sex or small-
scale spatial distribution, or for macrogeographic stock separation. 
These results are consistent with a single panmictic population within 
the northern Caribbean basin with high gene flow through the region.
    A recent study, published subsequent to the Biological Report, 
analyzed genetic variation in mtDNA, microsatellites, and single 
nucleotide polymorphisms for Nassau grouper (Jackson et al. 2014). The 
study identified three potential ``permeable'' barriers to dispersal 
and concluded that large-scale oceanographic patterns likely influence 
larval dispersal and population structuring (regional genetic 
differentiation). However, the evidence of population structuring was 
limited. In pairwise analyses of genetic distance between the sample 
populations (using Fst for microsatellites and [Fcy]st for mtDNA), zero 
(of 171) comparisons based on microsatellite DNA were statistically 
signficant, only 47 (of 153) comparisons based on mtDNA were 
statistically significant (p < 0.00029), and there was no indication of 
isolation by distance in any of the genetic datasets. Overall, while 
this study indicated some instances of genetic differentiation, the 
results do not indicate a high degree of population structuring across 
the range. When the Jackson et al. study is considered in the context 
of the larger body of literature, there remains some uncertainty as to 
population substructuring for Nassau grouper.

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). While it is taxonomically similar to other hermaphroditic 
groupers, the Nassau grouper is now primarily considered a gonochore 
with separate sexes (Sadovy and Colin 1995). Juveniles were found to 
possess both male and female tissue, indicating they can mature 
directly into either sex (Sadovy and Colin 1995). Other characteristics 
such as the strong size overlap between males and females, the presence 
of males that develop directly from the juvenile phase, the 
reproductive behavior of forming spawning aggregations, and the mating 
system were found to be inconsistent with the protogynous reproductive 
strategy (Colin 1992, Sadovy and Colin 1995).
    Both male and female Nassau grouper typically mature at 4-5 years 
of age and at lengths between 40 and 45 cm SL (44 and 50 cm TL). Size, 
rather than age, may be the major determinant of sexual maturation 
(Sadovy and Eklund 1999).

[[Page 42273]]

Nassau grouper raised from eggs in captivity matured at 40-45 cm SL 
(44-50 cm TL) in just over 2 years (Tucker and Woodward 1994). Yet, the 
minimum age at sexual maturity based on otoliths is between 4 and 8 
years (Bush et al. 1996, 2006). Most fish have spawned by age 7+ years 
(Bush et al. 2006).
    Fecundity estimates vary by location throughout the Caribbean. Mean 
fecundity estimates are generally between 3 and 5 eggs/mg of ripe 
ovary. For example, Carter et al. (1994) found female Nassau grouper 
between 30-70 cm SL 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). Estimated number of eggs in the ripe ovary 
(90.7 g) of a 44.5 cm 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 based 
only on vitellogenic oocytes, from fish captured in the Bahamas 
indicated a mean relative fecundity of 2.9 eggs/mg ripe ovary (s.d. = 
1.09; n = 64) and a mean egg production of 716,664 (range = 11,724-
4,327,440 for females between 47.5-68.6 cm SL). Estimates of oocyte 
production from Nassau grouper induced to spawn in captivity are closer 
to the lower estimates based solely on vitellogenic oocyte counts.

Spawning Behavior and Habitat

    Nassau grouper form spawning aggregations at predictable locations 
around the winter full moons, 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 (Figure 10 in Hill and Sadovy de Mitcheson 2013). Recent 
evidence suggests that spawning is occurring at what may 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, despite the fact 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 movements of adult Nassau grouper from coral 
reefs to spawning aggregation sites, were first described in 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; some fish move 
only a few kilometers (km), while others move up to several hundred km 
(Colin 1992, Carter et al. 1994, Bolden 2000). Ongoing research in the 
Exuma Sound, Bahamas has tracked migrating Nassau grouper up to 200 km, 
with likely estimates of up to 330 km, 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 2 out of 22 tagged 
fish returning to home reefs in the Bahamas one year after 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 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 same 
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 1999, 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. Researchers speculate the location of spawning sites 
assists 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 study around a spawning aggregation site at 
Little Cayman, surface velocity profile drifters released on the night 
of peak spawning tended to remain near or returned to the spawning reef 
due to eddy formation, while drifters released on the days preceding 
the peak spawn tended to move away from the reef in line with the 
dominant currents (Heppell et al. 2011).
    Spawning aggregations form around the full moon between December 
and March (reviewed in Sadovy and Eklund 1999), though this may occur 
later (May-August) in more northerly latitudes (La Gorce 1939, Bardach 
et al. 1958, Smith 1971, Burnett-Herkes 1975). The formation of 
spawning aggregations is triggered by a very narrow range of water 
temperatures between 25[deg]-26 [deg]C. While day length has also been 
considered as a trigger for aggregation formation (Colin 1992, Tucker 
et al. 1993, Carter et al. 1994), temperature is evidently a more 
important stimulus (Hill and Sadovy de Mitcheson 2013). The narrow 
range of water temperature is likely responsible for the later 
reproductive season in more northerly latitudes like Bermuda.
    Spawning occurs for up to 1.5 hours around sunset for several days 
(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

[[Page 42274]]

spawning activity later occurs (Colin 1992, Kadison et al. 2010, Nemeth 
2012). Courtship is indicated by two behaviors that occur late in the 
afternoon: ``following'' and ``circling'' (Colin 1992). The aggregation 
then moves into deeper water shortly before spawning (Colin 1992, 
Tucker et al. 1993, Carter et al. 1994). 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). Following the release of sperm and 
eggs, there is a rapid return of the fragmented sub-group to the 
bottom. All spawning events have been recorded within 20 minutes of 
sunset, with most within 10 minutes of sunset (Colin 1992).
    Repeated spawning occurs at the same site for up to three 
consecutive months generally around the full moon or between the full 
and new moons (Smith 1971, Colin 1992, Tucker et al. 1993, Aguilar-
Perera 1994, Carter et al. 1994, Tucker and Woodward 1994). 
Participation by individual fish across the months is unknown. 
Examination of female reproductive tissue suggests multiple spawning 
events across several days at a single aggregation (Smith 1972, Sadovy, 
NMFS, pers. obs.). A video recording shows a single female in repeated 
spawning rushes during a single night, repeatedly releasing eggs (Colin 
1992). It is unknown whether a single, mature female will spawn 
continuously throughout the spawning season or just once per 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 (the fishing mortality rate that 
produces a certain spawning potential ratio) = 35 percent on non-
spawning fish would be 50 percent of the fishing mortality of the 1998 
to 2001 level. The 5 percent and 95 percent confidence limits are 
estimated to be less than 20 percent and more than 100 percent 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 
percent (5 and 95 percent confidence interval (CI) of 20 and 30 
percent, respectively). This level is significantly below the reference 
limit of 35 percent 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 (i.e., the species is extinct for fishery purposes 
due to low catch per unit effort) in a number of 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, and 
85 percent of the Nassau grouper catch came 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 or more 
(Evermann 1900). The Nassau grouper was still the fourth-most common 
shallow-water species landed in Puerto Rico in the 1970s (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). By 
1986, the Nassau grouper was considered commercially extinct in the 
U.S. Caribbean (Bohnsack et al. 1986). About 1,000 kg of Nassau grouper 
landings were reported in the Puerto Rico Reef Fish Fishery during the 
latter half of the 1980s, and most of them were less than 50 cm 
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. Results from these monitoring studies offer some 
indication of relative abundance of Nassau grouper in various 
locations, 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, includes few 
reports of Nassau grouper, as sighting frequency (proportion of all 
surveys with at least one Nassau grouper present) ranged from less than 
1 percent to less than 10 percent per survey from 1997-2000. Density of 
Nassau grouper ranged 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 of Nassau grouper has ranged from 0 to 0.5 percent with 
density between 0 to 0.5 fish/hectare. Data from SCUBA surveys 
conducted by the University of the Virgin Islands report a density of 4 
Nassau grouper/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 of 2-10 percent per survey, with a 
density of 1 Nassau grouper/hectare (NOAA's NMFS FRVC). In addition to 
these surveys, Hodgson and Liebeler (2002) noted that Nassau grouper 
were absent from 82 percent of shallow Caribbean reefs surveyed (3-10 
m) during a 5-year period (1997-2001) for the ReefCheck project.

Fishing Impacts on Spawning Aggregations

    Because we lack sufficient stock assessments or population 
estimates, we considered the changes in spawning aggregations as a 
proxy for the status of the current population. We believe the

[[Page 42275]]

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. Historically, 50 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). Based on the size and number of current 
spawning aggregations the Nassau grouper population appears to be just 
a fraction of its historical size.
    In general, slow-growing, long-lived species (such as snappers and 
groupers) with limited spawning periods, and possibly with narrow 
recruitment windows, 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 repeated reports from across the Caribbean where Nassau 
grouper spawning aggregations have been discovered and fished to the 
point that the aggregation ceased to form, or formed at such low 
densities that spawning was no longer viable. For example, the 
commercial fishing of Nassau grouper aggregations in Bermuda resulted 
in decreased landings from 75,000 tons in 1975 to 10,000 tons by 1981 
(Luckhurst 1996, Sadovy de Mitcheson and Erisman 2012). The four known 
spawning aggregation sites in Bermuda ceased to form shortly thereafter 
and have yet to recover (Sadovy de Mitcheson and Erisman 2012). 
However, Nassau grouper are still present in Bermuda and reported 
observations have slightly increased over the last 10-15 years (B. 
Luckhurst, Bermuda Department of Agriculture, Fisheries, and Parks, 
Division of Fisheries, pers. comm. to Y. Sadovy, University of Hong 
Kong, 2012). In Puerto Rico, historical spawning aggregations no longer 
form, though a small aggregation has recently been found, and may be a 
reconstitution of one of the former aggregations (Sch[auml]rer et al. 
2012). In Mahahual, Quintana Roo, Mexico, aggregations of up to 15,000 
fish formed each year, but due to increased fishing pressure in the 
1990's, aggregations have not formed in Mahahual since 1996 (Aguilar-
Perera 2006). Inadequate enforcement of management measures designed to 
protect spawning aggregations in Mexico has further affected 
aggregations (Aguilar-Perera 2006), though at least three aggregation 
sites remain viable. In Cuba, Nassau grouper were almost exclusively 
targeted during aggregation formation; because of this, there have been 
severe declines in the number of Nassau grouper at 8 of the 10 
aggregations and moderate declines in the other 2 (Claro et al. 2009). 
Similar situations are known to have occurred 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).
    Overexploitation has also occurred in Belize. Between 1975 and 2001 
there was an 80 percent decline in the number of Nassau grouper (15,000 
fish to 3,000) at the Glover's Reef aggregation (Sala et al. 2001). 
Additionally, a 2001 assessment concluded that only 2 of the 9 
aggregation sites identified in 1994 remained viable, and those had 
been reduced from 30,000 fish to 3,000-5,000 fish (Heyman 2002). More 
recent monitoring (2003-2012) at the two sites at Glover's Reef 
indicates further declines in the sizes of these aggregations. A 
maximum of 800-3,000 Nassau grouper were counted per year at these 
sites over the ten years of monitoring (Belize SPAG Working Group 
2012).
    Further indicators of population decline through over-exploitation 
include reduced size and/or age of fish harvested compared to maximum 
sizes and ages. Nassau grouper can attain sizes of greater than 120 cm 
(Heemstra and Randall 1993, Humann and Deloach 2002, Froese and Pauly 
2010) and live as long as 29 years (Bush et al. 2006). However, it is 
unusual to obtain individuals of more than 12 years of age in exploited 
fisheries, and more heavily fished areas yield much younger fish on 
average. The maximum age estimates in heavily exploited areas are 
depressed--9 years in the U.S.V.I. (Olsen and LaPlace 1979), 12 years 
in northern Cuba, 17 years in southern Cuba (Claro et al. 1990), and 21 
years in the Bahamas (Sadovy and Colin 1995). Similarly, there is some 
indication that size at capture of both sexes declined in areas of 
higher exploitation versus unexploited populations within a specific 
region (Carter et al 1994). When exploitation is high, catches are 
largely comprised of juveniles. For example, most catches of Nassau 
grouper in heavily exploited areas of Puerto Rico, Florida (Sadovy and 
Eklund 1999), and Cuba (Espinosa 1980) consisted of juveniles. In 
exploited U.S.V.I. aggregations, harvest of Nassau grouper larger than 
70 cm TL was uncommon (Olsen and LaPlace 1979).
    While direct fishing of spawning aggregations was a primary driver 
of Nassau grouper population declines as indicated by the observed 
declines in spawning aggregations (Sadovy de Mitcheson and Erisman 
2012), other factors also affect abundance. For example, removal of 
adults from spawning runs and intensive capture of juveniles, either 
through direct targeting (e.g., spearfishing) or using small mesh traps 
or nets, also occur (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).

NMFS's Conclusions From the Biological Report

    The species is made up of a single population over its entire 
geographic range. As summarized above, 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 identified (Hinegardner and Rosen 1972, Sedberry et al. 1996, 
Hateley 2005). Although a recent study (Jackson et al. 2014) reported 
genetic differentiation, it does not provide evidence to support 
biological differences between populations. We believe further studies 
are needed to verify and expand upon the work presented by Jackson et 
al (2014). Based on the best available information, we conclude there 
is a single population of Nassau grouper throughout the Caribbean.
    The species has patchy abundance, with declines identified in many 
areas. The Biological Report describes the reduction in both size and 
number of spawning aggregations throughout the range. Patchy abundance 
throughout the range of a species is common due to differences in 
habitat quality/quantity or exploitation levels at different locations. 
However, dramatic, consistent declines of Nassau grouper have been 
noted throughout its range. In many areas throughout the Caribbean, the 
species is now considered commercially extinct and numerous spawning 
aggregations have been extirpated with no signs of recovery.
    The species possesses life history characteristics that increase 
vulnerability to harvest, including slow growth to a large size, late 
maturation, formation of large spawning aggregations, and occurrence in 
shallow

[[Page 42276]]

habitat. This conclusion is based on the Description of the Species in 
the Biological Report (Hill and Sadovy de Mitcheson 2013). Slow growth 
and late maturation expose 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 thus heavily exploited. 
Despite these life-history vulnerabilities, there are remaining 
spawning aggregations that, while reduced in size and number, still 
function and provide recruits into the population.
    The species is broadly distributed, and its current range is 
similar to its historical range. The Range-wide Distribution section of 
the Biological Report (Hill and Sadovy de Mitcheson 2013) concluded 
that the current range is equivalent to the historical range, though 
abundance has been severely depleted.

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.
    Members of the ERAG 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 the upper estimate of generation time for Nassau grouper (9-10 
years) as described by Sadovy and Eklund (1999) and an age at maturity 
of 8 years (Bush et al. 1996, 2006). We chose 30 years, which would 
potentially allow recruitment of 2-3 generations of mature individuals 
to appear in spawning aggregations as a result of fishery management 
actions. Given the limited information we have to predict the impacts 
of threats, we felt the 30 year timeframe was the most appropriate to 
assess threats in the foreseeable future.
    Members of the ERAG 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. Each member of 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. We did not directly relate the 
risk levels with particular listing outcomes, because the risk levels 
alone are not very informative. Acknowledging the differences in 
terminology between the ERAG risk scale and the ESA statutory 
definitions of threatened and endangered, we relied upon our own 
judgment and expertise in reviewing the ERA to determine the status of 
Nassau grouper and form our final listing determination.
    ERAG members were also asked to consider the potential interactions 
between demographic factors and threats. If the demographic factor or 
threat was ranked higher due to interactions with other demographic 
factors or threats, each member was asked to then 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., the 
Convention on International Trade in Endangered Species (CITES), as 
described in the Biological Report) were categorized by the ERAG 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), fishing at 
spawning aggregations, and inadequate law enforcement were classified 
as ``high risk.'' The demographic factors and threats are described 
below by the five ESA factors with the corresponding ERAG ranking and 
our analysis.

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

    Spatial structure/connectivity and habitat alteration were 
considered under ESA 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 alteration was 
ranked by the ERAG as a ``low risk'' threat to Nassau grouper. We agree 
with the ERAG that habitat alteration presents a low risk to the 
species and is unlikely to contribute to the threat of extinction 
presently or over the foreseeable future. The use of many different 
habitat types by Nassau grouper may spread the risk of impacts 
associated with habitat loss to a point that reduces overall extinction 
risk to the species.
    The range of Nassau grouper is influenced by spatial structure and 
connectivity of the population. 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, in part, to the declining number and size of spawning 
aggregations, which affects population structure. Given the increasing 
risk associated with this demographic factor we believe it could lead 
the species to become endangered over the foreseeable future.

[[Page 42277]]

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

    Based on ERAG rankings, historical harvest and fishing at spawning 
aggregations are two of the three most severe threats (the third being 
inadequate law enforcement) to Nassau grouper. Historical harvest and 
fishing at 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. We believe this lower ranking may be related 
to the fact that the species has declined to the point that commercial 
harvest is not as large a threat as in decades past. This is also 
related to abundance which was similarly classified as a ``moderate'' 
risk for Nassau grouper.
    Two different aspects of fishing affect Nassau grouper abundance: 
Fishing effort throughout the non-spawning months and directed fishing 
at spawning aggregations or on migrating adults. In some countries 
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 spawning 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 1980s and early 1990s 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 spawning aggregations continue 
throughout the Nassau grouper's range (Sadovy de Mitcheson 2012).
    We agree with the ERAG's assessment for the threat of abundance. It 
is clear that the abundance of Nassau grouper has diminished 
dramatically over the past several decades. This decline is a direct 
impact of historical harvest and the overfishing of spawning 
aggregations. The current abundance of Nassau grouper is not causing or 
contributing to the species currently being in danger of extinction but 
does raise concern for the status of the species over the foreseeable 
future if abundance continues to decline.
    We disagree with the ERAG's ``high risk'' rating for historical 
harvest. We believe that while historical harvest has reduced the 
population size of Nassau grouper, which has in turn affected the 
ability of the population to recover, we don't agree that this threat 
continues to be a ``high risk''. It seems more appropriate to consider 
the ERAG's risk assessment for the abundance of the current population 
in making our listing determination.
    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) was likely a result of 
overharvesting fish from spawning aggregations (Olsen and LaPlace 1979, 
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 population size. It appears that 
fishing at spawning aggregations has depressed population size such 
that fishing operations away from the aggregations are also impacting 
population status.
    We agree that fishing at spawning aggregations has reduced the 
population of Nassau grouper and has affected its current status. While 
the ERAG determined this is a ``high risk'' threat, we are less certain 
about our determination. We believe that this threat is in large part 
exacerbated by the inadequacy of regulatory mechanisms as discussed 
further below under Factor D. If existing regulatory mechanisms and 
corresponding law enforcement were adequate, this threat would be less 
of a concern. In the absence of adequate law enforcement, we believe 
that fishing at spawning aggregations is increasing the extinction risk 
of Nassau grouper.
    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. We recognize the uncertainty 
associated with this threat and believe more information is needed. 
That said, we do not believe available information indicates artificial 
selection is currently impacting the species' risk of extinction.

C. Disease

    There is very little information on the impacts of disease, 
parasites, and abnormalities on Nassau grouper, yet the species is not 
known to be affected by any specific disease or parasite. Given this, 
NMFS agrees with the ERAG ranking indicating a ``very low risk'' threat 
from disease, parasites, and abnormalities. We do not believe any of 
these threats will rise to the level of impacting the species' status 
over the foreseeable future.

D. Inadequacy of Existing Regulatory Mechanisms

    Consideration of the inadequacy of existing regulatory mechanisms, 
includes whether enforcement of those mechanisms is adequate. The 
relevance of existing regulatory mechanisms to extinction risk for an 
individual species depends on the vulnerability of that species to each 
of the threats identified under the other factors of ESA section 4, and 
the extent to which regulatory mechanisms could or do control the 
threats that are contributing to the species' extinction risk. If a 
species is not currently, and not expected within the foreseeable 
future to become, vulnerable to a particular threat, it is not 
necessary to evaluate the adequacy of existing regulatory mechanisms 
for addressing that threat. Conversely, if a species is vulnerable to a 
particular threat (now or in the foreseeable future), we do evaluate 
the adequacy of existing measures, if any, in controlling or mitigating 
that threat. In the following paragraphs, we will discuss existing 
regulatory mechanisms for addressing the threats to Nassau grouper 
generally, and assess their adequacy for controlling those threats. In 
the Extinction Risk Analysis section, we determine if the inadequacy of 
regulatory mechanisms is a contributing factor to the species' status 
as threatened or endangered because the existing regulatory mechanisms 
fail to adequately control or mitigate the underlying threats.
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 and

[[Page 42278]]

thus maintain abundance. Existing regulatory mechanisms include minimum 
size restrictions, seasonal closures, spatial closures, and gear and 
access restrictions. We summarize some of these regulatory mechanisms 
below by country.
    The Bahamas has implemented a number of regulatory mechanisms to 
limit harvest. 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. Up until 2015, the 
implementation of the 3-month closure was determined annually and could 
be shortened or otherwise influenced by such factors as the economy 
(Sadovy and Eklund 1999). In 2015, the annual assessment of the closure 
was removed ensuring a fixed 3-month closure each year moving forward 
(Fisheries Resources [Jurisdiction and Conservation] [Amendment] 
Regulations 2015). 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.
    The Bahamas has implemented several other actions that aid the 
conservation of Nassau grouper. There are marine parks in the Bahamas 
that are closed to fishing year round 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 in the Bahamas are also 
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 later introduced (Hill and Sadovy de 
Mitcheson 2013 and citations therein).
    In 2001 the Belize National Spawning Aggregation Working Group 
established protective legislation for 11 of the known Nassau grouper 
spawning sites within Belize. 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). In 2003, Belize introduced a four-month closed season to 
protect spawning fish (O'Connor 2002, Gibson 2008). However, the 2003 
legislation also allowed for exemptions to the closures by special 
license granted by the Fisheries Administrator, provided data be taken 
on any Nassau grouper removed. These special licenses made it difficult 
to enforce the national prohibition and in 2010 Belize stopped issuing 
permits to fish for Nassau grouper during the 4-month spawning period, 
except at Maugre Caye and Northern Two Caye.
    In 2009, Belize issued additional protective measures to help 
manage and protect the Nassau grouper. These include minimum and 
maximum size limits of 20 inches and 30 inches, respectively. Belize 
has also introduced a plan to ban 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-inch by 
2-inch skin patch (The Belize Spawning Aggregation Working Group 2009). 
Other gear restrictions are in place to generally aid in the management 
of reef fish, 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 
included and continued to be fished. In 1990, a two-fish bag limit and 
minimum size restriction (35.6 cm 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 Cayman Islands, the three main (``traditional'') grouper 
``holes'' were officially protected in the late 1970's and only 
residents were allowed to fish by lines during the spawning season 
(Hill and Sadovy de Mitcheson 2013). 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).
    Following the development of the monitoring program, the Cayman 
Islands implemented a number of management measures. In the early 
1990s, legislation prohibited spearfishing at spawning aggregation 
sites. In 1998, the three main grouper holes at the eastern end of the 
islands were formally designated as ``Restricted Marine Areas'' where 
access requires licensing by the Marine Conservation Board (Bush et al. 
2006). 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. A catch limit of 12 Nassau grouper per boat, per day during 
fishing years was also set. The 2002 law defined a one nautical mile 
(nm) ``no trapping'' zone around each spawning site, and set a minimum 
size limit of 12 inches for Nassau grouper 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 nm 
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 limit for Nassau grouper though 
this regulation is largely unprotective. The minimum size of 32 cm TL 
(or 570g) for Nassau grouper is less than the reported average size at 
maturity of 50 cm TL, indicating that Nassau grouper can be harvested 
before having the opportunity

[[Page 42279]]

to reproduce. Of some benefit to Nassau grouper are more general 
fishing regulations such as 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 also 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 
nationally.
    In Mexico, following scientific documentation of declines of Nassau 
grouper at Mahahual (Aguilar-Perera 1994), two regulations were 
enacted: (1) In 1993 spear-fishing was banned at any spawning 
aggregation site in southern Quintana Roo; and (2) in 1997 the fishing 
of any grouper species was banned during December and January (Aguilar-
Perera 2006). Then, 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 this 
closure also 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; yet at this time 
the plan has not been implemented.
    In the Turks and Caicos Islands, the only documented Nassau grouper 
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, protection of Nassau grouper habitat and 
spawning migration corridors on the narrow ledge of Caicos Bank is 
problematic as it would impose economic hardship on local fishers who 
depend on those areas for commercial species (e.g., spiny lobsters) and 
subsistence fishing (Rudd 2001).
    In U.S. federal waters, including those federal waters around 
Puerto Rico and the U.S.V.I., take and possession of Nassau grouper 
have been prohibited since 1990. Since 1993, a ban on fishing/
possessing Nassau grouper was implemented for the state of Florida and 
has since been enacted in all U.S. state waters. The species was fully 
protected in both state and federal waters of 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), was intended to protect red hind and 
their spawning aggregations, as well as a former Nassau grouper 
spawning site (Brown 2007). 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 filleting at sea was prohibited 
(Garc[iacute]a-Moliner and Sadovy 2008).
    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 the United Nations Educational, 
Scientific and Cultural Organization (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, 
2010).
    There are other Caribbean countries that have either few management 
measures in place or have yet to implement any conservation measures 
for Nassau grouper. 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, 
though 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 the Dominican 
Republic the catch and sale of ripe female Nassau grouper during the 
spawning season is not allowed (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. In Honduras, there is no legislation that 
controls fishing in the snapper/grouper fishery; however, traps and 
spears are illegal in the Bay Islands. There are no Nassau grouper 
special regulations in Jamaica; yet, some marine protected areas were 
designated in 2011.
Analysis of Existing Regulatory Mechanisms
    The ERAG considered several threats under Factor D including law 
enforcement, international trade regulations, foreign regulations in 
their jurisdictional waters, U.S. federal laws, and U.S. state and 
territorial laws. The ERAG determined that these threats substantially 
contribute to the overall risk to the species. Inadequate law 
enforcement was noted by several ERAG members as influencing their 
scoring for abundance, fishing of spawning aggregations, commercial 
harvest, and historical harvest. Inadequate law enforcement led to 
higher risk scores for each of these threats. The ERAG scored law 
enforcement as a ``high risk'' threat for Nassau grouper. ERAG rankings 
for the other threats were widely distributed. The inadequacy of 
foreign regulations in jurisdictional waters was considered an 
``increasing'' risk while the risk of international trade regulations 
was ``unknown.'' The remaining two categories of regulations (U.S. 
Federal and State of Florida/U.S. territory regulations) were 
considered ``low risk'' and ``moderate risk'' respectively. While the 
ERAG rankings for threats impacting the adequacy of regulatory 
mechanisms were generally moderate, we believe the concern about 
fishing at spawning aggregations (``high risk'' according to the ERAG) 
is due in part to the inadequacy of existing regulatory mechanisms.
    Overall, we believe existing regulatory mechanisms throughout the 
species' range (international trade, foreign, U.S. federal, and U.S. 
state and territorial regulations) vary in their effectiveness, 
especially in addressing the most serious threat to Nassau grouper--
fishing of spawning aggregations. In some countries, an array of 
national regulatory mechanisms, increases in marine protected areas, 
and customary

[[Page 42280]]

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. In that 
park, there is a clear difference in the number, biomass, and size of 
Nassau grouper in comparison to adjacent areas where fishing is 
permitted (Sluka et al. 1997).
    We note, however, that many countries have few, if any, specific 
Nassau grouper regulations. Instead they rely on general fisheries 
regulations (e.g., Anguilla, Antigua-Barbuda, Colombia, and Cuba all 
rely only on size limits, while Guadeloupe and Martinique, Honduras, 
Jamaica, Mexico, St. Lucia, and the Turks and Caicos rely on a variety 
of general fishing regulations). Additionally, where Nassau grouper-
specific regulations do exist, the ERAG scores indicated that law 
enforcement still presents a high risk threat to the species. We agree 
with the ERAG's risk assessment and believe that law enforcement in 
many foreign countries is less than adequate, thus rendering the 
regulations ineffective.
    Some foreign regulations may be ephemeral, unprotective of 
migrating adults, or inadequate to conserve the viability of a species. 
In some cases, regulations do not completely protect all known spawning 
aggregations (e.g., Belize, where 2 spawning aggregations are fished by 
license). In another instance, we found no protections for Nassau 
grouper in any foreign country during the period they move to and from 
spawning aggregation sites. Foreign regulations in some countries 
specify exemptions for ``historical,'' ``local,'' or artisanal 
fishermen (e.g., Colombia). Finally, some particular types of 
regulations are insufficient to protect the species (e.g., minimum size 
limits in both the Bahamas and Cuba are less than size-at-maturity).
    In some places, such as Bermuda, no recovery has been documented 
after 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 potential recovery at spawning aggregation 
sites, but fishing continues to keep the population depressed (Semmens 
et al. 2012) and inconsistent surveys do not provide data adequate to 
realize impacts. Additionally, larval recruitment is highly variable 
due to currents in the Caribbean basin. Some populations may receive 
larval input from neighboring spawning aggregations, while other local 
circulation patterns may entrain larvae (Colin et al. 1987) making the 
population entirely self-recruiting.
    In conclusion, although many countries have taken regulatory 
measures to conserve Nassau grouper, the species faces an ongoing 
threat due to the inadequacy of regulatory mechanisms to prevent or 
remediate the impacts of other threats that are elevating the species' 
extinction risk, particularly fishing of spawning aggregations.

E. Other Natural or Manmade Factors Affecting Its Continued Existence

    The ERAG considered climate change as a threat 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 (Colin 1992, Tucker and Woodward 1996). Because Nassau 
grouper spawn in a narrow window of temperatures, a rise in sea surface 
temperature outside that range could impact spawning or shift the 
geographic range of it to overlap with waters within the required 
temperature parameters. Increased sea surface temperatures have also 
been linked to coral loss through bleaching and disease. Further, 
increased global temperatures are also predicted to change parasite-
host relationships and may present additional unknown concerns (Harvell 
et al. 2002, Marcogliese 2001). Rising sea surface temperatures are 
also associated with sea level rise. If sea level changed rapidly, 
water depth at reef sites may be modified with such rapidity that coral 
and coral reefs could be affected (Munday et al. 2008).
    Another potential effect of climate change could be the loss of 
structural habitat in coral reef ecosystems as ocean acidification is 
anticipated to affect the integrity of coral reefs (Munday et al. 
2008). Bioerosion may reduce the 3-dimensional structure of coral reefs 
(Alvarez-Filip et al. 2009), reducing adult habitat for Nassau grouper 
(Coleman and Koenig 2010, Rogers and Beets 2001). Results of the ERAG 
scores indicated that climate change was an ``unknown risk'' to Nassau 
grouper. We agree with the assessment of the ERAG and believe there is 
not enough information at this time to determine how climate change is 
affecting the extinction risk of Nassau grouper now or in the 
foreseeable future.
    The ERAG also considered threats from aquaculture to Nassau grouper 
under Factor E and determined that aquaculture was a ``very low'' risk 
threat to Nassau grouper. Experiments to determine the success rate of 
larval Nassau grouper culture (Watanabe et al. 1995a, 1995b) and 
survival of released hatchery-reared juveniles have been conducted and 
feasibility of restocking reefs has been tested (Roberts et al. 1995) 
in St. Thomas, U.S.V.I. However, 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 introducing Nassau grouper raised in facilities, 
possible problems of juvenile habitat availability, introduction of 
maladapted individuals, and the inability of stocked individuals to 
locate traditional spawning locations, continue to be raised. Given the 
number of concerns with aquaculture and the fact that some spawning 
aggregations remain, we believe that it is unlikely that Nassau grouper 
aquaculture will develop further. Therefore we agree with the ERAG that 
aquaculture presents a very low extinction risk to Nassau grouper and 
is not contributing to the species' current status.
    Demographic factors of abundance, population growth rate/
productivity and diversity were also considered by the ERAG under 
Factor E. Each ERAG member considered whether the species is likely to 
be able to maintain a sustainable population size and adequate genetic 
diversity. 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. Trends or shifts in demographic 
or reproductive traits were considered when assessing the ranking of 
threats by each ERAG member to identify a decline in population growth 
rate. The ERAG scores indicated that abundance of Nassau grouper was a 
``moderate risk,'' growth rate/productivity was an ``increasing risk,'' 
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.
NMFS's Conclusions From Threats Evaluation
    The most serious threats to Nassau grouper are fishing at spawning 
aggregations and inadequate law enforcement. These threats, considered 
under Factors B and D, were rated by the ERAG as ``high risk'' threats 
to the species. We agree with the ERAG's assessment that these threats 
are currently affecting the status of Nassau grouper, putting it at a 
heightened risk

[[Page 42281]]

of extinction. A variety of other threats were identified by the ERAG 
as also impacting the status of this species. Growth rate/productivity 
(Factor E), spatial structure/connectivity (Factors A and E), and 
effectiveness of foreign regulations (Factor D) were identified by the 
ERAG as ``increasing risks.'' Artificial selection (Factor B), 
abundance (Factors B and E), diversity (Factor E), commercial harvest 
(Factors B and D), and effectiveness of state and territory regulations 
(Factor D) were determined to be ``moderate risks.'' NMFS concurs that 
these threats have the potential to adversely affect the status of 
Nassau grouper over the foreseeable future.

Extinction Risk Analysis

    We must assess the ERA results and make a determination as to 
whether the Nassau grouper is currently in danger of extinction, or 
likely to become so within the foreseeable future. We first evaluated 
the current status of the Nassau grouper in light of the four 
demographic factors. Based on our assessment of the ERA in regards to 
these demographic factors (abundance, growth rate/productivity, spatial 
structure and connectivity, and diversity) we do not believe the Nassau 
grouper is currently in danger of extinction. Each of these demographic 
factors was ranked by the ERAG as a moderate or increasing risk to the 
species' current status.
    We acknowledge that the abundance of Nassau grouper has been 
dramatically reduced in relation to historical records, but we do not 
believe abundance is currently so low that the species is at risk of 
extinction from stochastic events, environmental variation, 
anthropogenic perturbations, lack of genetic diversity, or depensatory 
processes. Although the reduced abundance of Nassau grouper has 
diminished the size and number of spawning aggregations, spawning is 
still occurring and abundance is increasing in some locations (e.g. 
Cayman Islands and Bermuda) where adequate protections are effectively 
being implemented. The abundance of Nassau grouper is now patchily 
distributed throughout the Caribbean with areas of higher abundance 
correlated with those areas with effective regulations. We believe the 
abundance of Nassau grouper in these protected areas is large enough to 
sustain the overall population and limit extinction risk. However, we 
also believe that further regulations will be necessary in other 
countries to counteract past population declines and ultimately recover 
the population of Nassau grouper throughout the Caribbean.
    Abundance is closely related with the other three demographic 
factors. Growth rate/productivity, spatial structure and connectivity, 
and diversity are all negatively affected by decreased abundance 
associated with overexploitation. Historical overfishing has led to a 
decreased average length and earlier age at maturity in exploited 
populations, which affects the species' ability to maintain the 
population growth rate above replacement level. Reductions in the 
number and distribution of spawning aggregations has the potential to 
affect larval and juvenile dispersal. This can further affect genetic 
diversity within the population. However, we don't believe that any of 
these demographic factors have been adversely affected to the point 
that Nassau grouper is currently in danger of extinction. As described 
previously, the species continues to occupy its current range, spawning 
is still occurring in several locations thus continuing to deliver new 
recruits to the population, and recovery of spawning aggregations has 
been documented in locations with adequate regulatory mechanisms and 
enforcement. The size of Nassau grouper is also increasing in areas 
where protections are in place (e.g., Belize and U.S.V.I.), indicating 
that current abundance is not adversely affecting growth rate and 
productivity at these locations.
    After considering the current status of Nassau grouper based on the 
four demographic factors, we next assessed how the identified threats 
are expected to affect the status of the species, including its 
demographic factors, over the foreseeable future. The ERAG identified a 
variety of threats that have the potential to impact Nassau grouper. 
The ERAG ranked and we agreed that several threats (habitat alteration, 
disease, aquaculture, and U.S. federal regulations) ranked as ``very 
low'' or ``low'' risk, will have little to no effect on the extinction 
risk of Nassau grouper within the foreseeable future. Several other 
threats (commercial harvest, artificial selection, foreign regulations 
within jurisdictional waters, and regulations of the U.S. and its 
territories), were ranked as moderate or increasing risks to the status 
of Nassau grouper. We agree that collectively these threats could cause 
Nassau grouper to become in danger of extinction within the foreseeable 
future.
    Finally, the ERAG identified three threats that present a ``high'' 
risk to the status of Nassau grouper over the foreseeable future. We 
agree with the ERAG's assessment that fishing of spawning aggregations 
combined with inadequate law enforcement is currently adversely 
affecting the status of Nassau grouper as discussed above, but disagree 
with the ERAG's ranking of historic harvest as a high risk. These high 
risk threats will continue to elevate the extinction risk of Nassau 
grouper over the foreseeable future. Both threats directly affect the 
current abundance of the species, its ability to maintain population 
growth rate, the population structure of the species, and its diversity 
in terms of genetics and overall ecology.
    As previously described, the ERAG analyzed inadequate law 
enforcement as a standalone threat under Factor D, inadequacy of 
existing regulatory mechanisms, and ranked it as a ``high risk'' 
threat. We agree that existing regulations, and enforcement of existing 
regulations, are inadequate to control the threat posed by fishing on 
spawning aggregations, and thus this threat under Factor D is 
contributing to the extinction risk and status of Nassau grouper.
    Based on the information in the Biological Report and the results 
from the ERA, we conclude that ESA Factors B (overutilization for 
commercial, recreational, scientific, or educational purposes), D 
(inadequacy of regulatory mechanisms), and E (other natural or manmade 
factors) are contributing to a threatened status for Nassau grouper. 
Overutilization in the form of historical harvest has reduced 
population size and led to the collapse of spawning aggregations in 
many locations. While some countries have made efforts to curb harvest, 
fishing at spawning aggregation sites remains a ``high risk'' threat. 
Further contributing to the risk of Nassau grouper extinction is the 
inadequacy of regulatory control and law enforcement, which leads to 
continued overutilization (low abundance), reduced reproductive output, 
and reduced recruitment. If growth and sexual recruitment rates cannot 
balance the loss from these threats, populations will become more 
vulnerable to extinction over the future (Primack 1993).

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. To evaluate the efficacy of domestic efforts that have not 
yet implemented or that have been implemented, but have not yet 
demonstrated to be effective, the Services developed a joint ``Policy 
for Evaluation of Conservation Efforts When Making Listing Decisions'' 
(``PECE''; 68 FR 15100; March 28, 2003).

[[Page 42282]]

The PECE is designed to ensure consistent and adequate evaluation on 
whether domestic 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 unnecessary.
    The PECE establishes two overarching 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. While section 4(b)(1)(A) requires that 
we evaluate both domestic and foreign conservation efforts, it does not 
set out particular criteria for doing so. While the particular 
framework of the PECE policy only directly applies to consideration of 
domestic efforts, we have discretion to evaluate foreign efforts using 
a similar approach and find that it is reasonable to do so here. In our 
discretion, we evaluated foreign conservation efforts to protect and 
recover Nassau grouper that are either underway, but not yet fully 
implemented, or are only planned, using these overarching criteria.
    Conservation efforts with the potential to address identified 
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 known conservation efforts, 
including those that have yet to be fully implemented or have yet to 
demonstrate effectiveness. Conservation efforts that we considered that 
are yet to be fully implemented include 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 several years old with no updates or known 
implementation, we find that there is not a sufficient basis to 
conclude that there is a reasonable certainty of implementation or 
effectiveness. We also considered the marine protected areas 
implemented by Jamaica in 2011, though based on Jamaica's historic 
overfishing and difficulty in enforcing existing regulations, we find 
that there is not a sufficient basis to conclude that these marine 
protected areas present a reasonable certainty of effectiveness in 
reducing threats that contribute to Nassau grouper's extinction risk. 
We carefully considered the other conservation efforts summarized in 
the Biological Report and acknowledge that time is required to see the 
benefit of mature adults in the spawning aggregations; however, the 
continued decline in number and size of Nassau grouper spawning 
aggregations indicates the effectiveness of those conservation efforts 
is currently unknown and thus there is insufficient basis to conclude 
there is a reasonable certainty of effectiveness. While some 
conservation efforts have been partially successful on localized 
scales, Nassau grouper appear to still be overutilized and at 
heightened risk of extinction based on the ERA. After taking into 
account these conservation efforts, our evaluation of the section 
4(a)(1) factors is that the conservation efforts do not reduce the risk 
of extinction of Nassau grouper to the point at which listing is not 
warranted.

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 2014 Draft Policy with regards to the 
Nassau grouper and completed an assessment of potential ``SPOIR,'' 
which is documented in the ERA. However, throughout the status review 
process NMFS determined threats and risks to the status of Nassau 
grouper are affecting the species over the entirety of its range. 
Because the threats and risks are widespread throughout the entire 
range of this species, there is no portion of the range that can be 
considered ``significant.''

Listing Determination

    Based on the Biological Report, the Threats Evaluation, the 
Extinction Risk Analysis, and Protective Efforts we determined that the 
Nassau grouper warrants a threatened status under the ESA. 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 unregulated harvest; (3) historical harvest 
greatly diminished the population of Nassau grouper and the species has 
yet to recover from this overexploitation; (4) spawning aggregations 
have drastically declined in size and number across the species' range; 
(5) there are two threats the ERAG rated as ``high risk,'' that we 
agree are affecting the current status of the species and will continue 
to do so over the foreseeable future--fishing at spawning aggregations 
and inadequate law enforcement; and (6) historical harvest has abated, 
though existing regulatory mechanisms and law enforcement have not been 
effective in preventing fishing at many spawning aggregation sites. 
Conservation efforts in some nations (U.S., Puerto Rico, U.S.V.I., and 
Belize) have almost certainly prevented further declines. Given the 
life history characteristics of Nassau grouper, more time will be 
needed to determine if these protective measures are successful in 
recovering the population. Collectively, the information obtained 
during the status review indicates the species is not currently in 
danger of extinction

[[Page 42283]]

(though reduced in number, the species maintains its historical range 
and still forms spawning aggregations at some sites), but it is likely 
to become endangered within the foreseeable future (based on continued 
risk of harvest, especially at spawning aggregation sites inadequately 
controlled by regulations and law enforcement). Accordingly, we have 
determined that the Nassau grouper warrants listing as a threatened 
species under the ESA.

Effects of Listing

    Conservation measures provided for species listed as endangered or 
threatened under the ESA include recovery plans (16 U.S.C. 1533(f)), 
critical habitat designations (16 U.S.C. 1533(a)(3)(A)), Federal agency 
consultation requirements (16 U.S.C. 1536), and protective regulations 
(16 U.S.C. 1533(d)). 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. Both a 
recovery program and designation of critical habitat could result from 
this final listing. Given its broad range across the Caribbean Sea, a 
regional cooperative effort to protect and restore Nassau grouper is 
necessary. We anticipate that protective regulations for Nassau grouper 
will also be necessary for the conservation of the species. 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)(2) of the ESA and NMFS/FWS regulations require Federal 
agencies to consult with us on any actions 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 
practices.

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 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. Critical habitat 
may also include areas unoccupied by Nassau grouper if those areas are 
essential to the conservation of the species.
    Section 4(a)(3)(A) of the ESA (16 U.S.C. 1533(a)(3)(A)) requires 
that, to the maximum extent prudent and determinable, critical habitat 
be designated concurrently with the listing of a species. Pursuant to 
50 CFR 424.12(a), designation of critical habitat is not determinable 
when one or both of the following situations exist: Data sufficient to 
perform required analyses are lacking; or the biological needs of the 
species are not sufficiently well known to identify any area that meets 
the definition of ``critical habitat.'' Although we have gathered 
information through the status review and public comment periods on the 
habitats occupied by this species, we currently do not have enough 
information to determine what physical and biological features within 
those habitats facilitate the species' life history strategy and are 
thus essential to the conservation of Nassau grouper, and may require 
special management considerations or protection. 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.

Policies on Peer Review

    In December 2004, the Office of Management and Budget (OMB) issued 
a Final Information Quality Bulletin for Peer Review establishing 
minimum peer review standards, a transparent process for public 
disclosure of peer review planning, and opportunities for public 
participation. The OMB Bulletin, implemented under the Information 
Quality Act (Pub. L. 106-554) is intended to enhance the quality and 
credibility of the Federal government's scientific information, and 
applies to influential or highly influential scientific information 
disseminated on or after June 16, 2005. To satisfy our requirements 
under the OMB Bulletin, we obtained independent peer review of the 
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 final rule.

Solicitation of Information

    We are soliciting information on features and areas that may 
support designation of critical habitat for Nassau grouper. Information 
provided should identify the physical and biological features essential 
to the conservation of the species and areas that contain these 
features. Areas outside the occupied geographical area should also be 
identified if such areas themselves are essential to the conservation 
of the species. Essential features may include, but are not limited to, 
features specific to the species' range, habitats, and life history 
characteristics within the following general categories of habitat 
features: (1) Space for individual growth and for normal behavior; (2) 
food, water, air, light, minerals, or other nutritional or 
physiological requirements; (3) cover or shelter; (4) sites for 
reproduction and development of offspring; and (5) habitats that are 
protected from disturbance or are representative of the historical, 
geographical, and ecological distributions of the species (50 CFR 
424.12(b)). ESA implementing regulations at 50 CFR 424.12(h) specify 
that critical habitat shall not be

[[Page 42284]]

designated within foreign countries or in other areas outside of U.S. 
jurisdiction. Therefore, we request information only on potential areas 
of critical habitat within waters in U.S. jurisdiction.
    For features and areas potentially qualifying as critical habitat, 
we also request information describing: (1) Activities or other threats 
to the essential features or activities that could be affected by 
designating them as critical habitat, and (2) the positive and negative 
economic, national security and other relevant impacts, including 
benefits to the recovery of the species, likely to result if these 
areas are designated as critical habitat.

References

    A complete list of the references used in this final rule is 
available at: (http://sero.nmfs.noaa.gov/protected_resources/listing_petitions/species_esa_consideration/index.html).

Classifications

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 final rule is exempt from review under Executive 
Order 12866. This final rule does not contain a collection-of-
information requirement for the purposes of the Paperwork Reduction 
Act.

Executive Order 13132, Federalism

    In keeping with the intent of the Administration and Congress to 
provide continuing and meaningful dialogue on issues of mutual state 
and Federal interest, the proposed rule was provided to the relevant 
agencies in each state in which the subject species occurs, and these 
agencies were invited to comment. We did not receive comments from any 
state agencies.

Executive Order 12898, Environmental Justice

    Executive Order 12898 requires that Federal actions address 
environmental justice in the decision-making process. In particular, 
the environmental effects of the actions should not have a 
disproportionate effect on minority and low-income communities. This 
final rule is not expected to have a disproportionately high effect on 
minority populations or low-income populations.

List of Subjects in 50 CFR Part 223

    Endangered and threatened species, Exports, Transportation.

    Dated: June 21, 2016.
Samuel D Rauch, III,
Deputy Assistant Administrator for Regulatory Programs, National Marine 
Fisheries Service.

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

PART 223--THREATENED MARINE AND ANADROMOUS SPECIES

0
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).


0
2. In Sec.  223.102, amend the table in paragraph (e) by adding an 
entry under the ``Fishes'' subheading for ``Grouper, Nassau'' in 
alphabetical order to read as follows:


Sec.  223.102  Enumeration of threatened marine and anadromous species.

* * * * *
    (e) * * *

--------------------------------------------------------------------------------------------------------------------------------------------------------
                                         Species \1\
---------------------------------------------------------------------------------------------- Citation(s) for listing      Critical        ESA rules
          Common name                   Scientific name          Description of listed entity      determination(s)         habitat
--------------------------------------------------------------------------------------------------------------------------------------------------------
 
                                                                      * * * * * * *
            Fishes
 
                                                                      * * * * * * *
Grouper, Nassau...............  Epinephelus striatus..........  Entire species...............  [Insert Federal                      NA               NA
                                                                                                Register citation],
                                                                                                June 29, 2016.
 
                                                                      * * * * * * *
--------------------------------------------------------------------------------------------------------------------------------------------------------
\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).


[[Page 42285]]

* * * * *

[FR Doc. 2016-15101 Filed 6-28-16; 8:45 am]
BILLING CODE 3510-22-P



                                                42268            Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations

                                                also reduce, eliminate, or prevent                      the causing of them to be transported or               § 171.1 Applicability of Hazardous
                                                unnecessary differences in regulatory                   shipped is liable for a civil penalty of               Materials Regulations (HMR) to persons and
                                                requirements.                                           not more than $77,114 for each                         functions.
                                                  Similarly, the Trade Agreements Act                   violation, except the maximum civil                    *      *    *      *    *
                                                of 1979 (Pub. L. 96–39), as amended by                  penalty is $179,933 if the violation                      (g) Penalties for noncompliance. Each
                                                the Uruguay Round Agreements Act                        results in death, serious illness or severe            person who knowingly violates a
                                                (Pub. L. 103–465), prohibits Federal                    injury to any person or substantial                    requirement of the Federal hazardous
                                                agencies from establishing any                          destruction of property. There is no                   material transportation law, an order
                                                standards or engaging in related                        minimum civil penalty, except for a                    issued under Federal hazardous
                                                activities that create unnecessary                      minimum civil penalty of $463 for                      material transportation law, subchapter
                                                obstacles to the foreign commerce of the                violations relating to training. When the              A of this chapter, or a special permit or
                                                United States. For purposes of these                    violation is a continuing one, each day                approval issued under subchapter A or
                                                requirements, Federal agencies may                      of the violation constitutes a separate                C of this chapter is liable for a civil
                                                participate in the establishment of                     offense.                                               penalty of not more than $77,114 for
                                                international standards, so long as the                                                                        each violation, except the maximum
                                                                                                           (b) A person who knowingly violates
                                                standards have a legitimate domestic                                                                           civil penalty is $179,933 if the violation
                                                                                                        a requirement of the Federal hazardous
                                                objective, such as providing for safety,                                                                       results in death, serious illness or severe
                                                                                                        material transportation law, an order
                                                and do not operate to exclude imports                                                                          injury to any person or substantial
                                                                                                        issued thereunder, this subchapter,
                                                that meet this objective. The statute also                                                                     destruction of property. There is no
                                                                                                        subchapter C of the chapter, or a special
                                                requires consideration of international                                                                        minimum civil penalty, except for a
                                                                                                        permit or approval issued under this
                                                standards and, where appropriate, that                                                                         minimum civil penalty of $463 for a
                                                                                                        subchapter applicable to the design,
                                                they be the basis for U.S. standards.                                                                          violation relating to training.
                                                                                                        manufacture, fabrication, inspection,
                                                  PHMSA participates in the                             marking, maintenance, reconditioning,                    Issued in Washington, DC, on June 14,
                                                establishment of international standards                repair or testing of a package, container,             2016 under authority delegated in 49 CFR
                                                in order to protect the safety of the                   or packaging component which is                        part 1.97.
                                                American public, and we have assessed                   represented, marked, certified, or sold                Marie Therese Dominguez,
                                                the effects of the interim final rule to                by that person as qualified for use in the             Administrator, Pipeline and Hazardous
                                                ensure that it does not cause                           transportation of hazardous materials in               Materials Safety Administration.
                                                unnecessary obstacles to foreign trade.                 commerce is liable for a civil penalty of              [FR Doc. 2016–15404 Filed 6–28–16; 8:45 am]
                                                Accordingly, this rulemaking is                         not more than $77,114 for each                         BILLING CODE 4910–60–P
                                                consistent with Executive Order 13609                   violation, except the maximum civil
                                                and PHMSA’s obligations.                                penalty is $179,933 if the violation
                                                List of Subjects                                        results in death, serious illness or severe            DEPARTMENT OF COMMERCE
                                                                                                        injury to any person or substantial
                                                49 CFR Part 107                                         destruction of property. There is no                   National Oceanic and Atmospheric
                                                   Administrative practices and                         minimum civil penalty, except for a                    Administration
                                                procedure, Hazardous materials                          minimum civil penalty of $463 for
                                                transportation, Packaging and                           violations relating to training.                       50 CFR Part 223
                                                containers, Penalties, Reporting and                                                                           [Docket No. 1206013326–6497–03]
                                                                                                        ■ 3. In Appendix A to subpart D of part
                                                recordkeeping requirements.
                                                                                                        107, Section II.B. (‘‘Penalty Increases for            RIN 0648–XA984
                                                49 CFR Part 171                                         Multiple Counts’’), the first sentence of
                                                  General information, Regulations, and                 the second paragraph is revised to read                Endangered and Threatened Wildlife
                                                Definitions.                                            as follows:                                            and Plants: Final Listing Determination
                                                                                                                                                               on the Proposal To List the Nassau
                                                  In consideration of the foregoing, 49                 Appendix A to Subpart D of Part 107—
                                                                                                                                                               Grouper as Threatened Under the
                                                CFR Chapter I is amended as follows:                    Guidelines for Civil Penalties
                                                                                                                                                               Endangered Species Act
                                                                                                        *      *      *       *      *
                                                PART 107—HAZARDOUS MATERIALS                              Under the Federal hazmat law, 49 U.S.C.              AGENCY:  National Marine Fisheries
                                                PROGRAM PROCEDURES                                      5123(a), each violation of the HMR and each            Service (NMFS), National Oceanic and
                                                                                                        day of a continuing violation (except for              Atmospheric Administration (NOAA),
                                                ■  1. The authority citation for part 107               violations relating to packaging manufacture           Commerce.
                                                is revised to read as follows:                          or qualification) is subject to a civil penalty        ACTION: Final rule; request for
                                                  Authority: 49 U.S.C. 5101–5128, 44701;                of up to $77,114 or $179,933 for a violation           information.
                                                Pub. L. 101–410 section 4; Pub. L. 104–121,             occurring on or after August 1, 2016.
                                                sections 212–213; Pub. L. 104–134, section              *      *      *       *      *                         SUMMARY:    We, NMFS, are publishing
                                                31001; Pub. L. 114–74 section 4 (28 U.S.C.                                                                     this final rule to implement our
                                                2461 note); 49 CFR 1.81 and 1.97.                       PART 171—GENERAL INFORMATION,                          determination to list the Nassau grouper
                                                ■   2. Revise § 107.329 to read as follows:             REGULATIONS, AND DEFINITIONS                           (Epinephelus striatus) as threatened
                                                                                                                                                               under the Endangered Species Act of
                                                § 107.329   Maximum penalties.                          ■  4. The authority citation for part 171              1973, as amended (ESA). We have
                                                   (a) A person who knowingly violates                  is revised to read as follows:                         completed a status review of the Nassau
mstockstill on DSK3G9T082PROD with RULES




                                                a requirement of the Federal hazardous                                                                         grouper in response to a petition
                                                                                                          Authority: 49 U.S.C. 5101–5128, 44701;
                                                material transportation law, an order                   Pub. L. 101–410 section 4; Pub. L. 104–134,
                                                                                                                                                               submitted by WildEarth Guardians.
                                                issued thereunder, this subchapter,                     section 31001; Pub. L. 114–74 section 4 (28            After reviewing the best scientific and
                                                subchapter C of the chapter, or a special               U.S.C. 2461 note); 49 CFR 1.81 and 1.97.               commercial data available, including
                                                permit or approval issued under this                                                                           the status review and comments
                                                subchapter applicable to the                            ■ 5. In § 171.1, paragraph (g) is revised              received on the proposed rule, we have
                                                transportation of hazardous materials or                to read as follows:                                    determined that the Nassau grouper


                                           VerDate Sep<11>2014   16:45 Jun 28, 2016   Jkt 238001   PO 00000   Frm 00044   Fmt 4700   Sfmt 4700   E:\FR\FM\29JNR1.SGM   29JNR1


                                                                 Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations                                          42269

                                                meets the definition of a threatened                    Background                                             2012) and comments from three
                                                species. While the species still occupies                  On September 3, 2010, we received a                 independent peer reviewers. We used
                                                its historical range, overutilization                   petition from the WildEarth Guardians                  the Biological Report to complete a
                                                through historical harvest has reduced                  to list speckled hind (Epinephelus                     threats evaluation and an ERA to
                                                the number of individuals which in turn                 drummondhayi), goliath grouper (E.                     determine the status of the species.
                                                has reduced the number and size of                                                                                After completing the Biological
                                                                                                        itajara), and Nassau grouper (E. striatus)
                                                spawning aggregations. Although                                                                                Report and considering the information
                                                                                                        as threatened or endangered under the
                                                harvest of Nassau grouper has                                                                                  received on the 90-day finding, we
                                                                                                        ESA. The petition asserted that (1) the
                                                diminished due to management                                                                                   published a proposed rule to list Nassau
                                                                                                        present or threatened destruction,
                                                measures, the reduced number and size                                                                          grouper as a threatened species on
                                                                                                        modification, or curtailment of habitat
                                                of spawning aggregations and the                                                                               September 2, 2014 (79 FR 51929).
                                                                                                        or range; (2) overutilization for
                                                inadequacy of law enforcement                                                                                  During a 90-day comment period, we
                                                                                                        commercial, recreational, scientific, or
                                                continue to present extinction risk to                                                                         solicited comments on our proposal
                                                                                                        educational purposes; (3) inadequacy of
                                                Nassau grouper. Based on these                                                                                 from the public and any other interested
                                                                                                        existing regulatory mechanisms; and (4)
                                                considerations, described in more detail                                                                       parties.
                                                                                                        other natural or manmade factors are
                                                within this action, we conclude that the                                                                       Listing Determinations Under the ESA
                                                                                                        affecting the continued existence of and
                                                Nassau grouper is not currently in
                                                                                                        contributing to the imperiled statuses of                 We are responsible for determining
                                                danger of extinction throughout all or a
                                                                                                        these species. The petitioner also                     whether the Nassau grouper is
                                                significant portion of its range, but is
                                                                                                        requested that critical habitat be                     threatened or endangered under the
                                                likely to become so within the
                                                                                                        designated for these species concurrent                ESA (16 U.S.C. 1531 et seq.). Section
                                                foreseeable future. We also solicit
                                                                                                        with listing under the ESA. Due to the                 4(b)(1)(A) of the ESA requires us to
                                                information that may be relevant to the
                                                                                                        scope of the WildEarth Guardians’                      make listing determinations based
                                                designation of critical habitat for Nassau
                                                grouper, including information on                       petition, as well as the breadth and                   solely on the best scientific and
                                                physical or biological features essential               extent of the required evaluation and                  commercial data available after
                                                to the species’ conservation, areas                     response, we provided species-specific                 conducting a review of the status of the
                                                containing these features, and potential                90-day findings (76 FR 31592, June 1,                  species and after taking into account
                                                impacts of a designation.                               2011; 77 FR 25687, May 1, 2012; 77 FR                  efforts being made by any state or
                                                                                                        61559, October 10, 2012).                              foreign nation to protect the species. To
                                                DATES: The effective date of this final
                                                                                                           On October 10, 2012, we published a                 be considered for listing under the ESA,
                                                rule is July 29, 2016. Information on                   90-day finding for Nassau grouper with
                                                features, areas, and potential impacts,                                                                        a group of organisms must constitute a
                                                                                                        our determination that the petition                    ‘‘species,’’ which is defined in section 3
                                                that may support designation of critical                presented substantial scientific and
                                                habitat for Nassau grouper must be                                                                             of the ESA to include taxonomic species
                                                                                                        commercial information indicating that                 and ‘‘any subspecies of fish, or wildlife,
                                                received by August 29, 2016.                            the petitioned action may be warranted                 or plants, and any distinct population
                                                ADDRESSES: Information regarding this                   (77 FR 61559). At that time, we                        segment of any species of vertebrate fish
                                                final rule may be obtained by contacting                announced the initiation of a formal                   or wildlife which interbreeds when
                                                NMFS, Southeast Regional Office, 263                    status review and requested scientific                 mature.’’
                                                13th Avenue South, Saint Petersburg,                    and commercial information from the                       Section 3 of the ESA defines an
                                                FL 33701. Supporting information,                       public on: (1) The status of historical                endangered species as ‘‘any species
                                                including the Biological Report, is                     and current spawning aggregation sites;                which is in danger of extinction
                                                available electronically on the NMFS                    (2) historical and current distribution,               throughout all or a significant portion of
                                                Web site at: http://sero.nmfs.noaa.gov/                 abundance, and population trends; (3)                  its range’’ and a threatened species as
                                                protected_resources/listing_petitions/                  biological information (life history,                  one ‘‘which is likely to become an
                                                species_esa_consideration/index.html.                   genetics, population connectivity, etc.);              endangered species within the
                                                   You may submit information                           (4) management measures, regulatory                    foreseeable future throughout all or a
                                                regarding potential critical habitat                    mechanisms designed to protect                         significant portion of its range.’’ Thus,
                                                designation to the Protected Resources                  spawning aggregations, and enforcement                 we interpret an ‘‘endangered species’’ to
                                                Division by either of the following                     information; (5) any current or planned                be one that is presently in danger of
                                                methods:                                                activities that may adversely impact the               extinction. A ‘‘threatened species,’’ on
                                                   • Electronic Submissions: Submit all                 species; and (6) ongoing or planned                    the other hand, is not currently in
                                                electronic comments via the Federal                     efforts to protect and restore the species             danger of extinction but is likely to
                                                eRulemaking Portal. Go to                               and its habitat.                                       become so in the foreseeable future. In
                                                www.regulations.gov/                                       As part of the status review process to             other words, a key statutory difference
                                                #!docketDetail;D=NOAA-NMFS-2015-                        determine whether the Nassau grouper                   between a threatened and endangered
                                                0130, click the ‘‘Comment Now!’’ icon,                  warrants listing under the ESA, we                     species is the timing of when a species
                                                complete the required fields, and enter                 completed a Biological Report and an                   may be in danger of extinction, either
                                                or attach your comments.                                extinction risk analysis (ERA). The                    presently (endangered) or in the
                                                   • Mail: Submit written information to                Biological Report summarizes the                       foreseeable future (threatened).
                                                the Protected Resources Division, NMFS                  taxonomy, distribution, abundance, life                   Under section 4(a) of the ESA, we
                                                Southeast Regional Office, 263 13th                     history, and biology of the species. The               must determine whether any species is
                                                Avenue South, Saint Petersburg, FL                      Biological Report also identifies threats              endangered or threatened due to any of
                                                33701.
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                                                                                                        or stressors affecting the status of the               the following five factors: (A) The
                                                FOR FURTHER INFORMATION CONTACT:                        species as well as a description of the                present or threatened destruction,
                                                Adam Brame, NMFS, Southeast                             fisheries, fisheries management, and                   modification, or curtailment of its
                                                Regional Office (727) 209–5958; or Lisa                 conservation efforts. The Biological                   habitat or range; (B) overutilization for
                                                Manning, NMFS, Office of Protected                      Report incorporates information                        commercial, recreational, scientific, or
                                                Resources (301) 427–8466.                               received in response to our request for                educational purposes; (C) disease or
                                                SUPPLEMENTARY INFORMATION:                              information (77 FR 61559, October 10,                  predation; (D) the inadequacy of


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                                                42270            Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations

                                                existing regulatory mechanisms; or (E)                  endangered species list leads to                          Comment 4: Several comments
                                                other natural or manmade factors                        increased funding opportunities and                    indicated that spawning aggregation
                                                affecting its continued existence                       potential for collaboration between state              sites need to be protected and that
                                                (sections 4(a)(1)(A) through (E)). We are               and federal partners, as well as                       proper enforcement of both existing and
                                                required to make listing determinations                 stakeholders. We will seek regional                    future rules is paramount in protecting
                                                based solely on the best scientific and                 collaborative conservation efforts within              the species.
                                                commercial data available after                         the Caribbean region to further the                       Response: We agree that the lack of
                                                conducting a review of the status of the                conservation of the species.                           adequate protections for Nassau grouper
                                                species and after taking into account                      Comment 2: We received comments                     spawning aggregations and the
                                                efforts being made by any state or                      that the existing management measures                  inadequacy of law enforcement are
                                                foreign nation to protect the species.                  implemented by Fishery Management                      major contributors to the species’
                                                   In determining whether the Nassau                    Councils are already effective at                      decline throughout its range. These
                                                grouper meets the standard of                           protecting Nassau grouper within U.S.                  threats were rated ‘high’ during the ERA
                                                endangered or threatened, we followed                   waters, (including U.S. territorial waters             as explained in the proposed rule and,
                                                a stepwise approach. First we                           of Puerto Rico and the U.S. Virgin                     as such, were taken into consideration
                                                considered the specific life history,                   Islands) and that the listing may add                  when making our final listing
                                                ecology, and status of the species as                   unnecessary burdens on our domestic                    determination.
                                                documented in the Biological Report.                    fisheries.                                                Comment 5: One commenter
                                                We then considered information on                          Response: We agree that the South                   supported the rule stating, ‘‘We agree
                                                factors adversely affecting and posing                  Atlantic Fishery Management Council                    that the best available science
                                                extinction risk to the species in a threats             and the Caribbean Fishery Management                   demonstrates that Nassau grouper is
                                                evaluation. In this evaluation we                                                                              likely to be at risk of extinction in the
                                                                                                        Council have taken significant steps to
                                                assessed the threats affecting the status                                                                      foreseeable future, and may in fact be in
                                                                                                        protect and rebuild the Nassau grouper
                                                of the species using the factors                                                                               danger of extinction now.’’ They further
                                                                                                        population in U.S. waters.
                                                identified in ESA section 4(a)(1). We                                                                          encouraged swift designation of critical
                                                                                                        Unfortunately, a large part of the
                                                considered the nature of the threats and                                                                       habitat to protect spawning aggregation
                                                                                                        species’ range and population is outside
                                                the species response to those threats.                                                                         sites, nursery and juvenile habitat, and
                                                                                                        of U.S. jurisdiction and is therefore not
                                                We also considered each threat                                                                                 feeding habitat.
                                                                                                        directly aided by Council protections.                    Response: We acknowledge the
                                                identified, both individually and                       We must make our determination based
                                                cumulatively. Once we evaluated the                                                                            concern raised by the commenter that
                                                                                                        on the best scientific and commercial                  the species may be in danger of
                                                threats, we assessed the efforts being
                                                                                                        data available, independent of the                     extinction now and provide further
                                                made to protect the species to determine
                                                                                                        potential burdens to our other domestic                detail below as to how we reached our
                                                if these conservation efforts were
                                                                                                        fisheries. This standard has been                      listing determination in this final rule.
                                                adequate to mitigate the existing threats
                                                                                                        applied when making the Nassau                         With regard to critical habitat, section
                                                and alter extinction risk. Finally, we
                                                                                                        grouper final listing determination.                   4(a)(3)(A) of the ESA (16 U.S.C.
                                                considered the public comments
                                                received in response to the proposed                       Comment 3: Some comments                            1533(a)(3)(A)) requires that, if prudent
                                                rule. In making this finding, we have                   expressed concern over the economic                    and determinable, critical habitat be
                                                relied on the best available scientific                 consequences of listing Nassau grouper,                designated concurrently with the listing
                                                and commercial data.                                    including possible effects on                          of a species. We do not currently have
                                                                                                        commercial fishermen.                                  sufficient information to determine
                                                Summary of Comments Received                               Response: We are unable to consider                 what physical and biological features
                                                   Below we address the comments                        economic impacts in a listing                          within Nassau grouper habitats facilitate
                                                received on the proposed listing for                    determination. The ESA requires us to                  the species’ life history strategy and
                                                Nassau grouper. In response to our                      make listing determinations by                         thus are essential to the species’
                                                request for public comments, we                         evaluating the standards and factors in                conservation. Therefore, we cannot yet
                                                received 17 written responses. The                      section 4 of the ESA, and based solely                 determine what areas meet the
                                                overall feedback was supportive of the                  on the best scientific and commercial                  definition of critical habitat under the
                                                rule with the exception of three                        data available. Listing Nassau grouper as              ESA. Because critical habitat is not
                                                commenters, who believe current                         a threatened species would not create                  currently determinable, we will not
                                                regulations within the United States are                any immediate additional regulatory                    designate critical habitat concurrently
                                                sufficient in protecting this species. No               requirements directly affecting                        with this final rule. Designation of
                                                comments addressed threats to Nassau                    commercial fishermen. Potential future                 critical habitat may occur via a
                                                grouper throughout the rest of their                    regulations affecting conservation of                  subsequent rule-making process if we
                                                range. We did not receive any                           Nassau grouper, including take and                     can identify critical habitat and
                                                information on additional conservation                  import regulations may be proposed via                 designation is prudent. We are soliciting
                                                efforts being taken.                                    a separate rulemaking process which                    information on features, areas, and
                                                   Comment 1: Multiple commenters                       would include consideration of certain                 impacts of designation, that may
                                                supported the proposed rule to list                     economic impacts (e.g., impacts on                     support designation of critical habitat
                                                Nassau grouper as a threatened species                  small businesses) and opportunities for                for Nassau grouper.
                                                and further encouraged regional                         public input. Individuals that require                    Comment 6: One commenter
                                                collaboration to develop adequate                       federal permits or funding for actions                 suggested the use of size restrictions,
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                                                management measures.                                    that might affect Nassau grouper might                 monitoring, closed fishing seasons for
                                                   Response: We agree that regional                     need to make adjustments to their                      the protection of spawning aggregations,
                                                collaboration will strengthen efforts to                activities to avoid jeopardizing Nassau                and the use of marine protected areas as
                                                consistently manage and conserve the                    grouper, and to avoid or minimize take                 measures to protect the species.
                                                species, and we hope this listing will                  of the species, but that would be a                       Response: We summarize in this rule
                                                encourage collaborative efforts. In some                determination for a specific section 7                 the existing regulations currently in
                                                cases, adding a species to the                          consultation in the future.                            place throughout the Caribbean Sea that


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                                                                 Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations                                           42271

                                                include many of these suggested                         determinations based solely on the best                tail, and a row of black spots below and
                                                practices. Within U.S. waters, measures                 scientific and commercial data available               behind each eye. Color pattern can also
                                                to protect Nassau grouper are already in                after conducting a review of the status                change within minutes from almost
                                                place under the Magnuson-Stevens Act                    of the species and after taking into                   white to bicolored to uniformly dark
                                                and State and Territorial fishery                       account efforts being made by any state                brown, according to the behavioral state
                                                management authorities. As a species                    or foreign nation to protect the species.              of the fish (Longley 1917, Colin 1992,
                                                listed as threatened under the ESA, any                 We have not proposed any additional                    Heemstra and Randall 1993, Carter et al.
                                                federal action implemented, authorized                  regulations affecting management of                    1994). A distinctive bicolor pattern is
                                                or funded that ‘‘may affect’’ Nassau                    Nassau grouper as a result of the                      seen when two adults or an adult and
                                                grouper will require consultation to                    proposed listing rule. However, we will                large juvenile meet and is frequently
                                                ensure the action is not likely to                      need to determine whether we can                       observed at spawning aggregations
                                                jeopardize the species’ continued                       identify critical habitat for this species,            (Heemstra and Randall 1993). There is
                                                existence. We may also implement                        and if so, make an appropriate                         also a distinctive dark tuning-fork mark
                                                additional protective regulations for                   designation of critical habitat. A critical            that begins at the front of the upper jaw,
                                                Nassau grouper under section 4(d) of the                habitat designation could have                         extends back between the eyes, and then
                                                ESA if we determine such regulations                    implications for fishing activities. Any               divides into two branches on top of the
                                                are necessary and advisable for the                     designation of critical habitat would                  head behind the eyes. Another dark
                                                conservation of this threatened species.                include opportunities for public input.                band runs from the tip of the snout
                                                Issuance of a 4(d) rule would be a                      As previously mentioned, we could also                 through the eye and then curves upward
                                                separate rule-making process that would                 implement additional protective                        to meet its corresponding band from the
                                                include specific opportunities for public               regulations for Nassau grouper under                   opposite side just in front of the dorsal
                                                input.                                                  section 4(d) of the ESA, if we determine               fin. Juveniles exhibit a color pattern
                                                   Comment 7: The U.S. Navy identified                  they are necessary and advisable for the               similar to adults (e.g., Silva Lee 1977).
                                                three Navy installations or properties                  conservation of this threatened species.                  Maximum age has been estimated as
                                                that are within the geographic range of                 Issuance of a 4(d) rule would be a                     29 years, based on an ageing study using
                                                Nassau grouper. They expressed                          separate rule-making process that would                sagittal otoliths (Bush et al. 2006). Most
                                                concern over their ability to utilize and               include specific opportunities for public              studies indicate a rapid growth rate for
                                                maintain those areas with a listing and                 input.                                                 juveniles, which has been estimated to
                                                designation of critical habitat. In                                                                            be about 10 mm/month total length (TL)
                                                particular, the Navy expressed concern                  Changes From the Proposed Rule                         for small juveniles, and 8.4 to 11.7 mm/
                                                over their ability to conduct                             In addition to responding to the                     month TL for larger juveniles (Beets and
                                                maintenance dredging and requested we                   comments, we made a number of                          Hixon 1994, Eggleston 1995). Maximum
                                                consult with them prior to proposing                    changes in this final rule. These                      size is about 122 cm TL and maximum
                                                critical habitat.                                       included making revisions to the                       weight is about 25 kg (Heemstra and
                                                   Response: A rule to list Nassau                      Biological Review section (most notably                Randall 1993, Humann and Deloach
                                                grouper will require federal agencies to                in the Population Structure and                        2002, Froese and Pauly 2010).
                                                assess whether any actions                              Genetics, and the Fishing Impacts on                   Generation time (the interval between
                                                implemented, authorized, or funded                      Spawning Aggregations subsections),                    the birth of an individual and the
                                                within the range of the species ‘‘may                   including a more detailed description of               subsequent birth of its first offspring) is
                                                affect’’ Nassau grouper, and consult                    our role in the Threats Evaluation,                    estimated as 9–10 years (Sadovy and
                                                with NMFS to ensure their actions are                   providing more detail in the Extinction                Eklund 1999).
                                                not likely to jeopardize the species’                   Risk Analysis section, and clarifying the
                                                continued existence. The rule-making                                                                           Distribution
                                                                                                        role of foreign conservation measures as
                                                process for identifying critical habitat is             they relate to making our final listing                   The Nassau grouper’s confirmed
                                                separate from this final listing rule and               determination. We made several of these                distribution currently includes
                                                would include opportunities for public                  changes to provide clarity on how we                   ‘‘Bermuda and Florida (USA),
                                                participation and input, as well as                     reached our listing determination in                   throughout the Bahamas and Caribbean
                                                coordination with all military branches.                response to the comment that, ‘‘. . .                  Sea’’ (e.g., Heemstra and Randall 1993).
                                                Unlike ESA listing decisions, the                       Nassau grouper is likely to be at risk of              The occurrence of Nassau grouper from
                                                designation of critical habitat requires                extinction in the foreseeable future, and              the Brazilian coast south of the equator
                                                us to consider economic, national                       may in fact be in danger of extinction                 as reported in Heemstra and Randall
                                                security, and other impacts of the                      now.’’                                                 (1993) is ‘‘unsubstantiated’’ (Craig et al.
                                                designation.                                                                                                   2011). The Nassau grouper has been
                                                   Comment 8: One commenter opposed                     Biological Review                                      documented in the Gulf of Mexico, at
                                                the proposed rule to list Nassau grouper                   This section provides a summary of                  Arrecife Alacranes (north of Progreso) to
                                                as a threatened species stating this is                 key biological information presented in                the west off the Yucatan Peninsula,
                                                ‘‘merely a precursor to an attempt to                   the Biological Report (Hill and Sadovy                 Mexico, (Hildebrand et al. 1964).
                                                form a basis for a push for Marine                      de Mitcheson 2013), which provides the                 Nassau grouper is generally replaced
                                                Protection Areas.’’                                     baseline context and foundation for our                ecologically in the eastern Gulf by red
                                                   Response: The proposed rule to list                  listing determination.                                 grouper (E. morio) in areas north of Key
                                                Nassau grouper was the result of the                                                                           West or the Tortugas (Smith 1971). They
                                                petition we received from WildEarth                     Species Description                                    are considered a rare or transient
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                                                Guardians, our 90-day finding that the                    The Nassau grouper, E. striatus (Bloch               species off Texas in the northwestern
                                                petition presented substantial                          1792), is a long-lived, moderate sized                 Gulf of Mexico (Gunter and Knapp 1951
                                                information that listing may be                         serranid fish with large eyes and a                    in Hoese and Moore 1998). The first
                                                warranted, and our 12-month finding                     robust body. Coloration is variable, but               confirmed sighting of Nassau grouper in
                                                that listing as a threatened species was                adult fish are generally buff, with five               the Flower Garden Banks National
                                                warranted. Section 4(b)(1)(A) of the ESA                dark brown vertical bars, a large black                Marine Sanctuary, which is located in
                                                requires us to make listing                             saddle blotch on top of the base of the                the northwest Gulf of Mexico


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                                                42272            Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations

                                                approximately 180 km southeast of                       Nassau grouper in the Bahamas was                      single panmictic population within the
                                                Galveston, Texas, was reported by Foley                 18,305 m2 ± 5,806 (SD) with larger                     northern Caribbean basin with high
                                                et al. (2007). Many earlier reports of                  ranges at less structurally-complex reefs              gene flow through the region.
                                                Nassau grouper up the Atlantic coast to                 (Bolden 2001). The availability of                        A recent study, published subsequent
                                                North Carolina have not been                            habitat and prey was found to                          to the Biological Report, analyzed
                                                confirmed. The Biological Report (Hill                  significantly influence home range of                  genetic variation in mtDNA,
                                                and Sadovy de Mitcheson, 2013)                          adults (Bolden 2001).                                  microsatellites, and single nucleotide
                                                provides a detailed description of their                  Adult Nassau grouper tend to be                      polymorphisms for Nassau grouper
                                                distribution.                                           relatively sedentary and are generally                 (Jackson et al. 2014). The study
                                                                                                        associated with high-relief coral reefs or             identified three potential ‘‘permeable’’
                                                Habitat and Depth                                       rocky substrate in clear waters to depths              barriers to dispersal and concluded that
                                                   The Nassau grouper is primarily a                    of 130 m. Generally, adults are most                   large-scale oceanographic patterns likely
                                                shallow-water, insular fish species that                common at depths less than 100 m (Hill                 influence larval dispersal and
                                                has long been valued as a major fishery                 and Sadovy de Mitcheson, 2013) except                  population structuring (regional genetic
                                                resource throughout the wider                           when at spawning aggregations where                    differentiation). However, the evidence
                                                Caribbean, South Florida, Bermuda, and                  they are known to descend to depths of                 of population structuring was limited.
                                                the Bahamas (Carter et al. 1994). The                   255 m (Starr et al. 2007).                             In pairwise analyses of genetic distance
                                                Nassau grouper is considered a reef fish,                                                                      between the sample populations (using
                                                but it transitions through a series of                  Diet and Feeding
                                                                                                                                                               Fst for microsatellites and Ast for
                                                developmental shifts in habitat. As                        Adult Nassau grouper are                            mtDNA), zero (of 171) comparisons
                                                larvae, they are planktonic. After an                   unspecialized, bottom-dwelling,                        based on microsatellite DNA were
                                                average of 35–40 days and at an average                 ambush-suction predators (Randall                      statistically signficant, only 47 (of 153)
                                                size of 32 mm TL, larvae recruit from an                1965, Thompson and Munro 1978).                        comparisons based on mtDNA were
                                                oceanic environment into demersal                       Numerous studies describe adult Nassau                 statistically significant (p < 0.00029),
                                                habitats (Colin 1992, Eggleston 1995).                  grouper as piscivorous (Randall and                    and there was no indication of isolation
                                                Following settlement, juvenile Nassau                   Brock 1960, Randall 1965, Randall 1967,                by distance in any of the genetic
                                                grouper inhabit macroalgae (primarily                   Carter et al. 1994, Eggleston et al. 1998).            datasets. Overall, while this study
                                                Laurencia spp.), coral clumps (Porites                  Feeding can take place around the clock                indicated some instances of genetic
                                                spp.), and seagrass beds (Eggleston                     although most fresh food is found in                   differentiation, the results do not
                                                1995, Dahlgren 1998). Recently-settled                  stomachs collected in the early morning                indicate a high degree of population
                                                Nassau grouper have also been collected                 and at dusk (Randall 1967). Young                      structuring across the range. When the
                                                from rubble mounds, some from tilefish                  Nassau grouper (20.2–27.2 mm standard                  Jackson et al. study is considered in the
                                                (Malacanthus plumieri), at 18 m depth                   length; SL) feed on a variety of                       context of the larger body of literature,
                                                (Colin et al. 1997). Post-settlement,                   plankton, including pteropods,                         there remains some uncertainty as to
                                                small Nassau grouper have been                          amphipods, and copepods (Greenwood                     population substructuring for Nassau
                                                reported with discarded queen conch                     1991, Grover et al. 1998).                             grouper.
                                                shells (Strombus gigas) and other debris                Population Structure and Genetics
                                                around Thalassia beds (Randall 1983,                                                                           Reproductive Biology
                                                Eggleston 1995).                                          Early genetic analyses indicated high                   The Nassau grouper was originally
                                                   Juvenile Nassau grouper (12–15 cm                    gene flow throughout the geographic                    considered to be a monandric
                                                TL) are relatively solitary and remain in               range of Nassau grouper but were                       protogynous hermaphrodite, meaning
                                                specific areas for months (Bardach                      unable to determine the relative                       males derive from adult females that
                                                1958). Juveniles of this size class are                 contributions of populations                           undergo a change in sex (Smith 1971,
                                                associated with macroalgae, and both                    (Hinegardner and Rosen 1972, Hateley                   Claro et al. 1990, Carter et al. 1994).
                                                natural and artificial reef structure. As               2005). A study of Nassau grouper                       While it is taxonomically similar to
                                                juveniles grow, they move progressively                 genetic population structure, using                    other hermaphroditic groupers, the
                                                to deeper areas and offshore reefs                      mitochondrial DNA (mtDNA) and                          Nassau grouper is now primarily
                                                (Tucker et al. 1993, Colin et al. 1997).                nuclear microsatellite DNA, revealed no                considered a gonochore with separate
                                                Schools of 30–40 juveniles (25–35 cm                    clearly defined population                             sexes (Sadovy and Colin 1995).
                                                TL) were observed at 8–10 m depths in                   substructuring based on samples from                   Juveniles were found to possess both
                                                the Cayman Islands (Tucker et al. 1993).                Belize, Cuba, Bahamas, and Florida.                    male and female tissue, indicating they
                                                No clear distinction can be made                        These data indicated that spawning                     can mature directly into either sex
                                                between types of adult and juvenile                     aggregations are not exclusively self-                 (Sadovy and Colin 1995). Other
                                                habitats, although a general size                       recruiting and that larvae can disperse                characteristics such as the strong size
                                                segregation with depth occurs—with                      over great distances, but the relative                 overlap between males and females, the
                                                smaller Nassau grouper in shallower                     importance of self-recruitment and                     presence of males that develop directly
                                                inshore waters (3.7–16.5 m) and larger                  larval immigration to local populations                from the juvenile phase, the
                                                individuals more common on deeper                       was unclear (Sedberry et al. 1996).                    reproductive behavior of forming
                                                (18.3–54.9 m) offshore banks (Bardach                   Similarly, a study by Hateley (2005) that              spawning aggregations, and the mating
                                                et al. 1958, Cervigón 1966, Silva Lee                  analyzed samples from Belize, Bahamas,                 system were found to be inconsistent
                                                1974, Radakov et al. 1975, Thompson                     Turks and Caicos, and Cayman Islands                   with the protogynous reproductive
                                                and Munro 1978).                                        using enzyme electrophoresis indicated                 strategy (Colin 1992, Sadovy and Colin
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                                                   Recent work by Nemeth and                            low to intermediate levels of genetic                  1995).
                                                coworkers in the U. S. Virgin Islands                   variability. Results from this study                      Both male and female Nassau grouper
                                                (U.S.V.I.; manuscript, in prep) found                   provided no evidence for population                    typically mature at 4–5 years of age and
                                                more overlap in home ranges of smaller                  substructuring by sex or small-scale                   at lengths between 40 and 45 cm SL (44
                                                juveniles compared to larger juveniles                  spatial distribution, or for                           and 50 cm TL). Size, rather than age,
                                                and adults have larger home ranges with                 macrogeographic stock separation.                      may be the major determinant of sexual
                                                less overlap. Mean home range of adult                  These results are consistent with a                    maturation (Sadovy and Eklund 1999).


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                                                Nassau grouper raised from eggs in                      what may be reconstituted or novel                     (promontories) of the reef as little as 50
                                                captivity matured at 40–45 cm SL (44–                   spawning sites in both Puerto Rico and                 m from the shore, and close to a drop-
                                                50 cm TL) in just over 2 years (Tucker                  the U.S.V.I. (Hill and Sadovy de                       off into deep water over a wide (6–60 m)
                                                and Woodward 1994). Yet, the                            Mitcheson 2013). Suspected or                          depth range (Craig 1966, Smith 1972,
                                                minimum age at sexual maturity based                    anecdotal evidence also identifies                     Burnett-Herkes 1975, Olsen and LaPlace
                                                on otoliths is between 4 and 8 years                    spawning aggregations in Los Roques,                   1979, Colin et al. 1987, Carter 1989,
                                                (Bush et al. 1996, 2006). Most fish have                Venezuela (Boomhower et al. 2010) and                  Fine 1990, Beets and Friedlander 1998,
                                                spawned by age 7+ years (Bush et al.                    Old Providence in Colombia’s San                       Colin 1992, Aguilar-Perera 1994). Sites
                                                2006).                                                  Andrés Archipelago (Prada et al. 2004).               are characteristically small, highly
                                                  Fecundity estimates vary by location                  Neither aggregation nor spawning has                   circumscribed areas, measuring several
                                                throughout the Caribbean. Mean                          been reported from South America,                      hundred meters in diameter, with soft
                                                fecundity estimates are generally                       despite the fact ripe Nassau grouper are               corals, sponges, stony coral outcrops,
                                                between 3 and 5 eggs/mg of ripe ovary.                  frequently caught in certain areas (F.                 and sandy depressions (Craig 1966,
                                                For example, Carter et al. (1994) found                 Cervigón, Fundacion Cientifica Los                    Smith 1972, Burnett-Herkes 1975, Olsen
                                                female Nassau grouper between 30–70                     Roques-Venezuela, pers. comm. to Y.                    and LaPlace 1979, Colin et al. 1987,
                                                cm SL from Belize yielded a mean                        Sadovy, NMFS, 1991). Spawning                          Carter 1989, Fine 1990, Beets and
                                                relative fecundity of 4.1 eggs/mg ovary                 aggregation sites have not been reported               Friedlander 1999, Colin 1992, Aguilar-
                                                weight and a mean total number of                       in the Lesser Antilles, Central America                Perera 1994). Recent work has identified
                                                4,200,000 oocytes (range =                              south of Honduras, or Florida.                         geomorphological similarities in
                                                350,000¥6,500,000). Estimated number                       ‘‘Spawning runs,’’ or movements of                  spawning sites that may be useful in
                                                of eggs in the ripe ovary (90.7 g) of a                 adult Nassau grouper from coral reefs to               applying remote sensing techniques to
                                                44.5 cm SL Nassau grouper from                          spawning aggregation sites, were first                 discover previously unknown spawning
                                                Bermuda was 785,101 (Bardach et al.                     described in Cuba in 1884 by Vilaro                    sites (Kobara and Heyman 2010).
                                                1958). In the U.S.V.I., mean fecundity                  Diaz, and later by Guitart-Manday and                     The link between spawning sites and
                                                was 4.97 eggs/mg of ovary (s.d. = 2.32)                 Juarez-Fernandez (1966). Nassau                        settlement sites is also not well
                                                with mean egg production of 4,800,000                   grouper migrate to aggregation sites in                understood. Researchers speculate the
                                                eggs (Olsen and LaPlace 1979); however,                 groups numbering between 25 and 500,                   location of spawning sites assists
                                                this may be an overestimate as it                       moving parallel to the coast or along                  offshore transport of fertilized eggs.
                                                included premature eggs that may not                    shelf edges or even inshore reefs (Colin               However, currents nearby aggregation
                                                develop. Fecundity estimates based only                 1992, Carter et al. 1994, Aguilar-Perera               sites do not necessarily favor offshore
                                                on vitellogenic oocytes, from fish                      and Aguilar-Davila 1996, Nemeth et al.                 egg transport, indicating some locations
                                                captured in the Bahamas indicated a                     2009). Distance traveled by Nassau                     may be at least partially self-recruiting
                                                mean relative fecundity of 2.9 eggs/mg                  grouper to aggregation sites is highly                 (e.g., Colin 1992). In a study around a
                                                ripe ovary (s.d. = 1.09; n = 64) and a                  variable; some fish move only a few                    spawning aggregation site at Little
                                                mean egg production of 716,664 (range                   kilometers (km), while others move up                  Cayman, surface velocity profile drifters
                                                = 11,724¥4,327,440 for females                          to several hundred km (Colin 1992,                     released on the night of peak spawning
                                                between 47.5–68.6 cm SL). Estimates of                  Carter et al. 1994, Bolden 2000).                      tended to remain near or returned to the
                                                oocyte production from Nassau grouper                   Ongoing research in the Exuma Sound,                   spawning reef due to eddy formation,
                                                induced to spawn in captivity are closer                Bahamas has tracked migrating Nassau                   while drifters released on the days
                                                to the lower estimates based solely on                  grouper up to 200 km, with likely                      preceding the peak spawn tended to
                                                vitellogenic oocyte counts.                             estimates of up to 330 km, as they move                move away from the reef in line with
                                                                                                        to aggregation sites (Hill and Sadovy de               the dominant currents (Heppell et al.
                                                Spawning Behavior and Habitat
                                                                                                        Mitcheson 2013).                                       2011).
                                                  Nassau grouper form spawning                             Observations suggest that individuals                  Spawning aggregations form around
                                                aggregations at predictable locations                   can return to their original home reef                 the full moon between December and
                                                around the winter full moons, or                        following spawning. Bolden (2001)                      March (reviewed in Sadovy and Eklund
                                                between full and new moons (Smith                       reported 2 out of 22 tagged fish                       1999), though this may occur later
                                                1971, Colin 1992, Tucker et al. 1993,                   returning to home reefs in the Bahamas                 (May–August) in more northerly
                                                Aguilar-Perera 1994, Carter et al. 1994,                one year after spawning. Sonic tracking                latitudes (La Gorce 1939, Bardach et al.
                                                Tucker and Woodward 1994).                              studies around Little Cayman Island                    1958, Smith 1971, Burnett-Herkes 1975).
                                                Aggregations consist of hundreds,                       have demonstrated that spawners may                    The formation of spawning aggregations
                                                thousands, or, historically, tens of                    return to the aggregation site in                      is triggered by a very narrow range of
                                                thousands of individuals. Some                          successive months with returns to their                water temperatures between 25°–26 °C.
                                                aggregations have persisted at known                    residential reefs in between (Semmens                  While day length has also been
                                                locations for periods of 90 years or more               et al. 2007). Sixty percent of fish tagged             considered as a trigger for aggregation
                                                (see references in Hill and Sadovy de                   at the west end spawning aggregation                   formation (Colin 1992, Tucker et al.
                                                Mitcheson 2013). Pair spawning has not                  site in Little Cayman in January 2005                  1993, Carter et al. 1994), temperature is
                                                been observed.                                          returned to the same aggregation site in               evidently a more important stimulus
                                                  About 50 individual spawning                          February 2005 (Semmens et al. 2007).                   (Hill and Sadovy de Mitcheson 2013).
                                                aggregation sites have been recorded,                   Larger fish are more likely to return to               The narrow range of water temperature
                                                mostly from insular areas in the                        aggregation sites and spawn in                         is likely responsible for the later
                                                Bahamas, Belize, Bermuda, British                       successive months than smaller fish                    reproductive season in more northerly
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                                                Virgin Islands, Cayman Islands, Cuba,                   (Semmens et al. 2007).                                 latitudes like Bermuda.
                                                Honduras, Jamaica, Mexico, Puerto                          It is not known how Nassau grouper                     Spawning occurs for up to 1.5 hours
                                                Rico, Turks and Caicos, and the U.S.V.I.;               select and locate aggregation sites or                 around sunset for several days (Whaylen
                                                however, many of these may no longer                    why they aggregate to spawn. Spawning                  et al. 2007). At spawning aggregation
                                                form (Figure 10 in Hill and Sadovy de                   aggregation sites are typically located                sites, Nassau grouper tend to mill
                                                Mitcheson 2013). Recent evidence                        near significant geomorphological                      around for a day or two in a ‘‘staging
                                                suggests that spawning is occurring at                  features, such as projections                          area’’ adjacent to the core area where


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                                                42274            Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations

                                                spawning activity later occurs (Colin                   potential ratio) = 35 percent on non-                  LaPlace 1979). By 1981, ‘‘the Nassau
                                                1992, Kadison et al. 2010, Nemeth                       spawning fish would be 50 percent of                   grouper ha[d] practically disappeared
                                                2012). Courtship is indicated by two                    the fishing mortality of the 1998 to 2001              from the local catches and the ones that
                                                behaviors that occur late in the                        level. The 5 percent and 95 percent                    d[id] appear [were] small compared
                                                afternoon: ‘‘following’’ and ‘‘circling’’               confidence limits are estimated to be                  with previous years’’ (CFMC 1985). By
                                                (Colin 1992). The aggregation then                      less than 20 percent and more than 100                 1986, the Nassau grouper was
                                                moves into deeper water shortly before                  percent of the fishing mortality at the                considered commercially extinct in the
                                                spawning (Colin 1992, Tucker et al.                     1998 to 2001 level, respectively. In other             U.S. Caribbean (Bohnsack et al. 1986).
                                                1993, Carter et al. 1994). Progression                  words, if (1) fishing mortality (F) rates              About 1,000 kg of Nassau grouper
                                                from courtship to spawning may depend                   of non-spawning fish are maintained at                 landings were reported in the Puerto
                                                on aggregation size, but generally fish                 the 1998 to 2001 level, and (2) fishing                Rico Reef Fish Fishery during the latter
                                                move up into the water column, with an                  on spawning aggregations is negligible,                half of the 1980s, and most of them were
                                                increasing number exhibiting the                        the median spawning potential                          less than 50 cm indicating they were
                                                bicolor phase (Colin 1992, Carter et al.                (spawner biomass relative to the                       likely sexually immature (Sadovy 1997).
                                                1994).                                                  unexploited level) is expected to be                      A number of organizations and
                                                   Spawning involves a rapid horizontal                 around 25 percent (5 and 95 percent                    agencies have conducted surveys to
                                                swim or a ‘‘rush’’ of bicolor fish                      confidence interval (CI) of 20 and 30                  examine the status of coral reefs and
                                                following dark fish closely in either a                 percent, respectively). This level is                  reef-fish populations throughout the
                                                column or cone rising to within 20–25                   significantly below the reference limit of             western Atlantic. Results from these
                                                m of the water surface where group-                     35 percent of spawning potential,                      monitoring studies offer some
                                                spawning occurs in sub-groups of 3–25                   meaning that there is a high chance of                 indication of relative abundance of
                                                fish (Olsen and LaPlace 1979, Carter                    recruitment overfishing because of the                 Nassau grouper in various locations,
                                                1986, Aguilar-Perera and Aguilar-Davila                 low spawning stock biomass.’’                          although different methods are often
                                                1996). Following the release of sperm                      The Nassau grouper was formerly one                 employed and thus results of different
                                                and eggs, there is a rapid return of the                of the most common and important                       studies cannot be directly compared
                                                fragmented sub-group to the bottom. All                 commercial groupers in the insular                     (Kellison et al. 2009). The Atlantic and
                                                spawning events have been recorded                      tropical western Atlantic and Caribbean                Gulf Rapid Reef Assessment Program
                                                within 20 minutes of sunset, with most                  (Smith 1978, Randall 1983, Appeldoorn                  (AGRRA), which samples a broad
                                                within 10 minutes of sunset (Colin                      et al. 1987, Sadovy 1997). Declines in                 spectrum of western Atlantic reefs,
                                                1992).                                                  landings and catch per unit of effort                  includes few reports of Nassau grouper,
                                                   Repeated spawning occurs at the same                 (CPUE) have been reported throughout                   as sighting frequency (proportion of all
                                                site for up to three consecutive months                 its range, and it is now considered to be              surveys with at least one Nassau
                                                generally around the full moon or                       commercially extinct (i.e., the species is             grouper present) ranged from less than
                                                between the full and new moons (Smith                   extinct for fishery purposes due to low                1 percent to less than 10 percent per
                                                1971, Colin 1992, Tucker et al. 1993,                   catch per unit effort) in a number of                  survey from 1997–2000. Density of
                                                Aguilar-Perera 1994, Carter et al. 1994,                areas, including Jamaica, Dominican                    Nassau grouper ranged from 1 to 15
                                                Tucker and Woodward 1994).                              Republic, U.S.V.I., and Puerto Rico                    fish/hectare with a mean of 5.6 fish/
                                                Participation by individual fish across                 (Sadovy and Eklund 1999). Information                  hectare across all areas surveyed
                                                the months is unknown. Examination of                   on past and present abundance and                      (AGRRA). NOAA’s Coral Reef
                                                female reproductive tissue suggests                     density, at coral reefs and aggregation                Ecosystem Monitoring Program
                                                multiple spawning events across several                 sites, is based on a combination of                    (CREMP) has conducted studies on coral
                                                days at a single aggregation (Smith 1972,               anecdotal accounts, visual census                      reefs in Puerto Rico and the U.S.V.I.
                                                Sadovy, NMFS, pers. obs.). A video                      surveys, and fisheries data. Because                   since 2000, and sighting frequency of
                                                recording shows a single female in                      grouper species are reported collectively              Nassau grouper has ranged from 0 to 0.5
                                                repeated spawning rushes during a                       in landings data, there are limited                    percent with density between 0 to 0.5
                                                single night, repeatedly releasing eggs                 species-specific data to determine catch               fish/hectare. Data from SCUBA surveys
                                                (Colin 1992). It is unknown whether a                   of Nassau grouper throughout its range.                conducted by the University of the
                                                single, mature female will spawn                           While fisheries dependent data are                  Virgin Islands report a density of 4
                                                continuously throughout the spawning                    generally limited for the species                      Nassau grouper/hectare per survey
                                                season or just once per year.                           throughout its range, there are some                   across reef habitat types in the U.S.V.I.
                                                                                                        1970s and 1980s port-sampling data                     SCUBA surveys by NOAA in the Florida
                                                Status Assessments
                                                                                                        from the U.S.V.I. and Puerto Rico. In the              Keys across reef habitat types have
                                                   Few formal stock assessments have                    U.S.V.I., Nassau grouper accounted for                 sighting frequencies of 2–10 percent per
                                                been conducted for the Nassau grouper.                  22 percent of total grouper landings, and              survey, with a density of 1 Nassau
                                                The most recent published assessment,                   85 percent of the Nassau grouper catch                 grouper/hectare (NOAA’s NMFS FRVC).
                                                conducted in the Bahamas, indicates                     came from spawning aggregations (D.                    In addition to these surveys, Hodgson
                                                fishing effort, and hence fishing                       Olsen, Chief Scientist—St. Thomas                      and Liebeler (2002) noted that Nassau
                                                mortality (F), in the Bahamas needs to                  Fishermen’s Association, pers. comm. to                grouper were absent from 82 percent of
                                                be reduced from the 1998–2001 levels,                   J. Rueter, NMFS, October 2013). The                    shallow Caribbean reefs surveyed (3–10
                                                otherwise the stocks are likely to be                   first U.S. survey of the fishery resources             m) during a 5-year period (1997–2001)
                                                overexploited relative to biological                    of Puerto Rico noted the Nassau grouper                for the ReefCheck project.
                                                reference points (Cheung et al. 2013).                  was common and a very important food
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                                                The population dynamic modeling by                      fish, reaching a weight of 22.7 kg or                  Fishing Impacts on Spawning
                                                Cheung et al. (2013) found: ‘‘assuming                  more (Evermann 1900). The Nassau                       Aggregations
                                                that the closure of the spawning                        grouper was still the fourth-most                        Because we lack sufficient stock
                                                aggregation season is perfectly                         common shallow-water species landed                    assessments or population estimates, we
                                                implemented and enforced, the median                    in Puerto Rico in the 1970s (Thompson                  considered the changes in spawning
                                                value of FSPR (the fishing mortality rate               1978), and it was common in the reef                   aggregations as a proxy for the status of
                                                that produces a certain spawning                        fish fishery of the U.S.V.I. (Olsen and                the current population. We believe the


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                                                                 Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations                                           42275

                                                status of spawning aggregations is likely               aggregations have not formed in                        Cuba (Espinosa 1980) consisted of
                                                to be reflective of the overall population              Mahahual since 1996 (Aguilar-Perera                    juveniles. In exploited U.S.V.I.
                                                because adults migrate to spawning                      2006). Inadequate enforcement of                       aggregations, harvest of Nassau grouper
                                                aggregations for the only known                         management measures designed to                        larger than 70 cm TL was uncommon
                                                reproductive events. Historically, 50                   protect spawning aggregations in                       (Olsen and LaPlace 1979).
                                                spawning aggregation sites had been                     Mexico has further affected aggregations                  While direct fishing of spawning
                                                identified throughout the Caribbean                     (Aguilar-Perera 2006), though at least                 aggregations was a primary driver of
                                                (Sadovy de Mitcheson et al. 2008). Of                   three aggregation sites remain viable. In              Nassau grouper population declines as
                                                these 50, less than 20 probably still                   Cuba, Nassau grouper were almost                       indicated by the observed declines in
                                                remain (Sadovy de Mitcheson et al.                      exclusively targeted during aggregation                spawning aggregations (Sadovy de
                                                2008). Furthermore, while numbers of                    formation; because of this, there have                 Mitcheson and Erisman 2012), other
                                                fish at aggregation sites once numbered                 been severe declines in the number of                  factors also affect abundance. For
                                                in the tens of thousands (30,000–                       Nassau grouper at 8 of the 10                          example, removal of adults from
                                                100,000 fish; Smith 1972), they have                    aggregations and moderate declines in                  spawning runs and intensive capture of
                                                now been reduced to less than 3,000 at                  the other 2 (Claro et al. 2009). Similar               juveniles, either through direct targeting
                                                those sites where counts have been                      situations are known to have occurred                  (e.g., spearfishing) or using small mesh
                                                made (Sadovy de Mitcheson et al. 2008).                 in the Bahamas, U.S.V.I., Puerto Rico,                 traps or nets, also occur (Hill and
                                                Based on the size and number of current                 and Honduras (Sadovy de Mitcheson                      Sadovy de Mitcheson 2013). In addition
                                                spawning aggregations the Nassau                        and Erisman 2012, see also Hill and                    to the high fishing pressure in some
                                                grouper population appears to be just a                 Sadovy de Mitcheson 2013).                             areas, poaching also appears to be
                                                fraction of its historical size.                           Overexploitation has also occurred in               affecting some populations (e.g., in the
                                                                                                        Belize. Between 1975 and 2001 there                    Cayman Islands; Semmens et al. 2012).
                                                   In general, slow-growing, long-lived
                                                                                                        was an 80 percent decline in the
                                                species (such as snappers and groupers)                                                                        NMFS’s Conclusions From the
                                                                                                        number of Nassau grouper (15,000 fish
                                                with limited spawning periods, and                                                                             Biological Report
                                                                                                        to 3,000) at the Glover’s Reef aggregation
                                                possibly with narrow recruitment                                                                                  The species is made up of a single
                                                                                                        (Sala et al. 2001). Additionally, a 2001
                                                windows, are susceptible to                                                                                    population over its entire geographic
                                                                                                        assessment concluded that only 2 of the
                                                overexploitation (Bannerot et al. 1987,                                                                        range. As summarized above, multiple
                                                                                                        9 aggregation sites identified in 1994
                                                Polovina and Ralston 1987). The strong                  remained viable, and those had been                    genetic analyses indicate that there is
                                                appeal of spawning aggregations as                      reduced from 30,000 fish to 3,000–5,000                high gene flow throughout the
                                                targets for fishing, their importance in                fish (Heyman 2002). More recent                        geographic range of the Nassau grouper,
                                                many seasonal fisheries, and the                        monitoring (2003–2012) at the two sites                and no clearly defined population
                                                apparent abundance of fish at                           at Glover’s Reef indicates further                     substructuring has been identified
                                                aggregations make spawning                              declines in the sizes of these                         (Hinegardner and Rosen 1972, Sedberry
                                                aggregations particularly susceptible to                aggregations. A maximum of 800–3,000                   et al. 1996, Hateley 2005). Although a
                                                over-exploitation. There are repeated                   Nassau grouper were counted per year                   recent study (Jackson et al. 2014)
                                                reports from across the Caribbean where                 at these sites over the ten years of                   reported genetic differentiation, it does
                                                Nassau grouper spawning aggregations                    monitoring (Belize SPAG Working                        not provide evidence to support
                                                have been discovered and fished to the                  Group 2012).                                           biological differences between
                                                point that the aggregation ceased to                       Further indicators of population                    populations. We believe further studies
                                                form, or formed at such low densities                   decline through over-exploitation                      are needed to verify and expand upon
                                                that spawning was no longer viable. For                 include reduced size and/or age of fish                the work presented by Jackson et al
                                                example, the commercial fishing of                      harvested compared to maximum sizes                    (2014). Based on the best available
                                                Nassau grouper aggregations in                          and ages. Nassau grouper can attain                    information, we conclude there is a
                                                Bermuda resulted in decreased landings                  sizes of greater than 120 cm (Heemstra                 single population of Nassau grouper
                                                from 75,000 tons in 1975 to 10,000 tons                 and Randall 1993, Humann and Deloach                   throughout the Caribbean.
                                                by 1981 (Luckhurst 1996, Sadovy de                      2002, Froese and Pauly 2010) and live                     The species has patchy abundance,
                                                Mitcheson and Erisman 2012). The four                   as long as 29 years (Bush et al. 2006).                with declines identified in many areas.
                                                known spawning aggregation sites in                     However, it is unusual to obtain                       The Biological Report describes the
                                                Bermuda ceased to form shortly                          individuals of more than 12 years of age               reduction in both size and number of
                                                thereafter and have yet to recover                      in exploited fisheries, and more heavily               spawning aggregations throughout the
                                                (Sadovy de Mitcheson and Erisman                        fished areas yield much younger fish on                range. Patchy abundance throughout the
                                                2012). However, Nassau grouper are still                average. The maximum age estimates in                  range of a species is common due to
                                                present in Bermuda and reported                         heavily exploited areas are depressed—                 differences in habitat quality/quantity or
                                                observations have slightly increased                    9 years in the U.S.V.I. (Olsen and                     exploitation levels at different locations.
                                                over the last 10–15 years (B. Luckhurst,                LaPlace 1979), 12 years in northern                    However, dramatic, consistent declines
                                                Bermuda Department of Agriculture,                      Cuba, 17 years in southern Cuba (Claro                 of Nassau grouper have been noted
                                                Fisheries, and Parks, Division of                       et al. 1990), and 21 years in the                      throughout its range. In many areas
                                                Fisheries, pers. comm. to Y. Sadovy,                    Bahamas (Sadovy and Colin 1995).                       throughout the Caribbean, the species is
                                                University of Hong Kong, 2012). In                      Similarly, there is some indication that               now considered commercially extinct
                                                Puerto Rico, historical spawning                        size at capture of both sexes declined in              and numerous spawning aggregations
                                                aggregations no longer form, though a                   areas of higher exploitation versus                    have been extirpated with no signs of
mstockstill on DSK3G9T082PROD with RULES




                                                small aggregation has recently been                     unexploited populations within a                       recovery.
                                                found, and may be a reconstitution of                   specific region (Carter et al 1994). When                 The species possesses life history
                                                one of the former aggregations (Schärer                exploitation is high, catches are largely              characteristics that increase
                                                et al. 2012). In Mahahual, Quintana Roo,                comprised of juveniles. For example,                   vulnerability to harvest, including slow
                                                Mexico, aggregations of up to 15,000                    most catches of Nassau grouper in                      growth to a large size, late maturation,
                                                fish formed each year, but due to                       heavily exploited areas of Puerto Rico,                formation of large spawning
                                                increased fishing pressure in the 1990’s,               Florida (Sadovy and Eklund 1999), and                  aggregations, and occurrence in shallow


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                                                42276            Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations

                                                habitat. This conclusion is based on the                risk,’’ ‘‘low risk,’’ ‘‘moderate risk,’’               connectivity, commercial harvest,
                                                Description of the Species in the                       ‘‘increasing risk,’’ ‘‘high risk,’’ or                 foreign regulations, artificial selection,
                                                Biological Report (Hill and Sadovy de                   ‘‘unknown.’’ ‘‘Very low risk’’ meant that              and diversity were ranked as ‘‘moderate
                                                Mitcheson 2013). Slow growth and late                   it is unlikely that the demographic                    risk’’ to ‘‘increasing risk.’’ Historical
                                                maturation expose sub-adults to harvest                 factor or threat affects the species’                  harvest (the effect of prior harvest on
                                                prior to reproduction. Sub-adult and                    overall status. ‘‘Low risk’’ meant that the            current population status), fishing at
                                                adult Nassau grouper form large                         demographic factor may affect species’                 spawning aggregations, and inadequate
                                                conspicuous spawning aggregations.                      status, but only to a degree that it is                law enforcement were classified as
                                                These aggregations are often in shallow                 unlikely that this factor significantly                ‘‘high risk.’’ The demographic factors
                                                habitat areas that are easily accessible to             elevates risk of extinction now or in the              and threats are described below by the
                                                fishermen and thus heavily exploited.                   future. ‘‘Moderate risk’’ meant that the               five ESA factors with the corresponding
                                                Despite these life-history vulnerabilities,             demographic factor or threat contributes               ERAG ranking and our analysis.
                                                there are remaining spawning                            significantly to long term risk of
                                                                                                                                                               A. The Present or Threatened
                                                aggregations that, while reduced in size                extinction, but does not constitute a
                                                                                                                                                               Destruction, Modification, or
                                                and number, still function and provide                  danger of extinction in the near future.
                                                                                                                                                               Curtailment of Its Habitat or Range
                                                recruits into the population.                           ‘‘Increasing risk’’ meant that the present
                                                   The species is broadly distributed,                  demographic risk or threat is low or                      Spatial structure/connectivity and
                                                and its current range is similar to its                 moderate, but is likely to increase to                 habitat alteration were considered under
                                                historical range. The Range-wide                        high risk in the foreseeable future if                 ESA Factor A; this included habitat loss
                                                Distribution section of the Biological                  present conditions continue. Finally,                  or degradation, and the loss of habitat
                                                Report (Hill and Sadovy de Mitcheson                    ‘‘high risk’’ meant that the demographic               patches, critical source populations,
                                                2013) concluded that the current range                  factor or threat indicates danger of                   subpopulations, or dispersal among
                                                is equivalent to the historical range,                  extinction in the near future. Each                    populations.
                                                though abundance has been severely                      member of the ERAG evaluated risk on                      Nassau grouper use many different
                                                depleted.                                               this scale, and we then interpreted these              habitat types within the coral reef
                                                                                                        rankings against the statutory language                ecosystem. The increase in urban,
                                                Threats Evaluation                                                                                             industrial, and tourist developments
                                                                                                        for threatened or endangered to
                                                   The threats evaluation was the second                determine the status of Nassau grouper.                throughout the species range impacts
                                                step in the process of making an ESA                    We did not directly relate the risk levels             coastal mangroves, seagrass beds,
                                                listing determination for Nassau grouper                with particular listing outcomes,                      estuaries, and live coral (Mahon 1990).
                                                as described above in ‘‘Listing                         because the risk levels alone are not                  Loss of juvenile habitat, such as
                                                Determinations under the ESA’’. The                     very informative. Acknowledging the                    macroalgae, seagrass beds, and
                                                Extinction Risk Analysis Group (ERAG),                  differences in terminology between the                 mangrove channels is likely to
                                                which consisted of 12 NOAA Fisheries                    ERAG risk scale and the ESA statutory                  negatively affect recruitment rates.
                                                Science Center and Regional Office                      definitions of threatened and                          Habitat alteration was ranked by the
                                                personnel, was asked to independently                   endangered, we relied upon our own                     ERAG as a ‘‘low risk’’ threat to Nassau
                                                review the Biological Report and assess                 judgment and expertise in reviewing the                grouper. We agree with the ERAG that
                                                4 demographic factors (abundance,                       ERA to determine the status of Nassau                  habitat alteration presents a low risk to
                                                growth rate/productivity, spatial                       grouper and form our final listing                     the species and is unlikely to contribute
                                                structure/connectivity, and diversity)                  determination.                                         to the threat of extinction presently or
                                                and 13 specific threats (see ERA Threat                    ERAG members were also asked to                     over the foreseeable future. The use of
                                                Table under supporting documents).                      consider the potential interactions                    many different habitat types by Nassau
                                                The group members were asked to                         between demographic factors and                        grouper may spread the risk of impacts
                                                provide qualitative scores based on their               threats. If the demographic factor or                  associated with habitat loss to a point
                                                perceived severity of each factor and                   threat was ranked higher due to                        that reduces overall extinction risk to
                                                threat.                                                 interactions with other demographic                    the species.
                                                   Members of the ERAG were asked to                    factors or threats, each member was                       The range of Nassau grouper is
                                                independently evaluate the severity,                    asked to then identify those factors or                influenced by spatial structure and
                                                scope, and certainty for these threats                  threats that caused them to score the                  connectivity of the population. As
                                                currently and in the foreseeable future                 risk higher or lower than it would have                described in Hill and Sadovy de
                                                (30 years from now). The foreseeable                    been if it were considered                             Mitcheson (2013), a study of genetic
                                                future was based on the upper estimate                  independently. We then examined the                    population structure in Nassau grouper
                                                of generation time for Nassau grouper                   independent responses from each ERAG                   revealed no clearly defined population
                                                (9–10 years) as described by Sadovy and                 member for each demographic factor                     substructuring at the geographic
                                                Eklund (1999) and an age at maturity of                 and threat and used the modal response                 locations sampled, i.e., Belize, Cuba,
                                                8 years (Bush et al. 1996, 2006). We                    to determine the level of threat to                    Bahamas, and Florida (Sedberry et al.
                                                chose 30 years, which would potentially                 Nassau grouper.                                        1996). Based on ERAG scores, spatial
                                                allow recruitment of 2–3 generations of                    Climate change and international                    structure/connectivity was
                                                mature individuals to appear in                         trade regulations (e.g., the Convention                characterized as an ‘‘increasing’’ risk for
                                                spawning aggregations as a result of                    on International Trade in Endangered                   Nassau grouper. We agree with the
                                                fishery management actions. Given the                   Species (CITES), as described in the                   ERAG ranking and believe this
                                                limited information we have to predict                  Biological Report) were categorized by                 increasing risk is due, in part, to the
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                                                the impacts of threats, we felt the 30                  the ERAG as ‘‘unknown.’’ Habitat                       declining number and size of spawning
                                                year timeframe was the most                             alteration, U.S. federal regulations,                  aggregations, which affects population
                                                appropriate to assess threats in the                    disease/parasites/abnormalities, and                   structure. Given the increasing risk
                                                foreseeable future.                                     aquaculture were ranked as ‘‘very low                  associated with this demographic factor
                                                   Members of the ERAG were asked to                    risk’’ to ‘‘low risk.’’ State/territorial              we believe it could lead the species to
                                                rank each of four demographic factors                   regulations, growth rate/productivity,                 become endangered over the foreseeable
                                                and 13 identified threats as ‘‘very low                 abundance, spatial structure/                          future.


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                                                                 Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations                                            42277

                                                B. Overutilization for Commercial,                      believe that while historical harvest has              grouper. We recognize the uncertainty
                                                Recreational, Scientific, or Educational                reduced the population size of Nassau                  associated with this threat and believe
                                                Purposes                                                grouper, which has in turn affected the                more information is needed. That said,
                                                   Based on ERAG rankings, historical                   ability of the population to recover, we               we do not believe available information
                                                harvest and fishing at spawning                         don’t agree that this threat continues to              indicates artificial selection is currently
                                                aggregations are two of the three most                  be a ‘‘high risk’’. It seems more                      impacting the species’ risk of extinction.
                                                severe threats (the third being                         appropriate to consider the ERAG’s risk
                                                                                                                                                               C. Disease
                                                inadequate law enforcement) to Nassau                   assessment for the abundance of the
                                                                                                        current population in making our listing                 There is very little information on the
                                                grouper. Historical harvest and fishing                                                                        impacts of disease, parasites, and
                                                at spawning aggregations were both                      determination.
                                                                                                           Predictable spawning aggregations                   abnormalities on Nassau grouper, yet
                                                classified as ‘‘high’’ risk threats to                                                                         the species is not known to be affected
                                                                                                        make Nassau grouper a vulnerable
                                                Nassau grouper. Curiously, the ERAG                                                                            by any specific disease or parasite.
                                                                                                        fishing target. In many places, annual
                                                rankings for commercial harvest, which                  landings for Nassau grouper were                       Given this, NMFS agrees with the ERAG
                                                often includes the fishing on spawning                  mostly from aggregation-fishing (e.g.,                 ranking indicating a ‘‘very low risk’’
                                                aggregations, were lower and indicated                  Claro et al. 1990, Bush et al. 2006).                  threat from disease, parasites, and
                                                current commercial harvest was a                        Because Nassau grouper are only known                  abnormalities. We do not believe any of
                                                ‘‘moderate’’ threat for Nassau grouper.                 to reproduce in spawning aggregations,                 these threats will rise to the level of
                                                We believe this lower ranking may be                    removing ripe individuals from the                     impacting the species’ status over the
                                                related to the fact that the species has                spawning aggregations greatly                          foreseeable future.
                                                declined to the point that commercial                   influences population dynamics and
                                                harvest is not as large a threat as in                                                                         D. Inadequacy of Existing Regulatory
                                                                                                        future fishery yields (Shapiro 1987).                  Mechanisms
                                                decades past. This is also related to                   Harvesting a species during its
                                                abundance which was similarly                           reproductive period increases adult                       Consideration of the inadequacy of
                                                classified as a ‘‘moderate’’ risk for                   mortality and diminishes juvenile                      existing regulatory mechanisms,
                                                Nassau grouper.                                         recruitment rates. The loss of adults and              includes whether enforcement of those
                                                   Two different aspects of fishing affect              the lack of recruitment greatly increase               mechanisms is adequate. The relevance
                                                Nassau grouper abundance: Fishing                       a species’ extinction risk. The collapse               of existing regulatory mechanisms to
                                                effort throughout the non-spawning                      of aggregations in many countries                      extinction risk for an individual species
                                                months and directed fishing at                          (Sadovy de Mitcheson 2012) was likely                  depends on the vulnerability of that
                                                spawning aggregations or on migrating                   a result of overharvesting fish from                   species to each of the threats identified
                                                adults. In some countries Nassau                        spawning aggregations (Olsen and                       under the other factors of ESA section
                                                grouper are fished commercially and                     LaPlace 1979, Aguilar-Perera 1994,                     4, and the extent to which regulatory
                                                recreationally throughout the year by                   Sadovy and Eklund 1999). As Semmens                    mechanisms could or do control the
                                                handline, longline, fish traps, spear                   et al. (2012) noted from the results of a              threats that are contributing to the
                                                guns, and gillnets (NMFS General                        mark-recapture study on Cayman Brac,                   species’ extinction risk. If a species is
                                                Canvas Landing System). Fishing at                      Cayman Island fishermen appear to                      not currently, and not expected within
                                                spawning aggregations is mainly                         catch sufficient adult grouper outside                 the foreseeable future to become,
                                                conducted by handlines or by fish traps,                the spawning season to seriously impact                vulnerable to a particular threat, it is not
                                                although gillnets were being used in                    population size. It appears that fishing               necessary to evaluate the adequacy of
                                                Mexico in the early to mid-1990s                        at spawning aggregations has depressed                 existing regulatory mechanisms for
                                                (Aguilar-Perera 2004). Declines in                      population size such that fishing                      addressing that threat. Conversely, if a
                                                landings, catch per unit effort (CPUE)                  operations away from the aggregations                  species is vulnerable to a particular
                                                and, by implication, abundance in the                   are also impacting population status.                  threat (now or in the foreseeable future),
                                                late 1980s and early 1990s occurred                        We agree that fishing at spawning                   we do evaluate the adequacy of existing
                                                throughout its range, which has led                     aggregations has reduced the population                measures, if any, in controlling or
                                                Nassau grouper to now be considered                     of Nassau grouper and has affected its                 mitigating that threat. In the following
                                                commercially extinct in a number of                     current status. While the ERAG                         paragraphs, we will discuss existing
                                                areas (Sadovy and Eklund 1999).                         determined this is a ‘‘high risk’’ threat,             regulatory mechanisms for addressing
                                                Population declines and loss of                         we are less certain about our                          the threats to Nassau grouper generally,
                                                spawning aggregations continue                          determination. We believe that this                    and assess their adequacy for
                                                throughout the Nassau grouper’s range                   threat is in large part exacerbated by the             controlling those threats. In the
                                                (Sadovy de Mitcheson 2012).                             inadequacy of regulatory mechanisms as                 Extinction Risk Analysis section, we
                                                   We agree with the ERAG’s assessment                  discussed further below under Factor D.                determine if the inadequacy of
                                                for the threat of abundance. It is clear                If existing regulatory mechanisms and                  regulatory mechanisms is a contributing
                                                that the abundance of Nassau grouper                    corresponding law enforcement were                     factor to the species’ status as
                                                has diminished dramatically over the                    adequate, this threat would be less of a               threatened or endangered because the
                                                past several decades. This decline is a                 concern. In the absence of adequate law                existing regulatory mechanisms fail to
                                                direct impact of historical harvest and                 enforcement, we believe that fishing at                adequately control or mitigate the
                                                the overfishing of spawning                             spawning aggregations is increasing the                underlying threats.
                                                aggregations. The current abundance of                  extinction risk of Nassau grouper.
                                                Nassau grouper is not causing or                           The final threat analyzed for Factor B              Summary of Existing Regulatory
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                                                contributing to the species currently                   was artificial selection. The ERAG                     Mechanisms
                                                being in danger of extinction but does                  scores indicated artificial selection was                As discussed in detail in the
                                                raise concern for the status of the                     a ‘‘moderate’’ threat; however, ranking                Biological Report (Hill and Sadovy de
                                                species over the foreseeable future if                  of this threat was widely distributed                  Mitcheson 2013), a wide array of
                                                abundance continues to decline.                         amongst ERAG members, indicating a                     regulatory mechanisms exists
                                                   We disagree with the ERAG’s ‘‘high                   high level of uncertainty about the                    throughout the range of Nassau grouper
                                                risk’’ rating for historical harvest. We                effects of artificial selection on Nassau              that are intended to limit harvest and


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                                                42278            Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations

                                                thus maintain abundance. Existing                       Minister, is prohibited. Commercial                    two-fish bag limit and minimum size
                                                regulatory mechanisms include                           fishing in the Bahamas is restricted to                restriction (35.6 cm FL) were enacted in
                                                minimum size restrictions, seasonal                     only the native population and, as a                   Bermuda (Luckhurst 1996). Since 1996,
                                                closures, spatial closures, and gear and                consequence, all vessels fishing within                Nassau grouper has been completely
                                                access restrictions. We summarize some                  the Bahamas Exclusive Fishery Zone                     protected through a prohibition on take
                                                of these regulatory mechanisms below                    must be fully owned by a Bahamian                      and possession and likely benefits from
                                                by country.                                             citizen residing in the Bahamas.                       numerous no-take marine reserves (Hill
                                                   The Bahamas has implemented a                           In Belize, the first measure to protect             and Sadovy de Mitcheson 2013).
                                                number of regulatory mechanisms to                      Nassau grouper was a seasonal closure                     In the Cayman Islands, the three main
                                                limit harvest. In the 1980s, the Bahamas                within the Glover’s Reef Marine Reserve                (‘‘traditional’’) grouper ‘‘holes’’ were
                                                introduced a minimum size of 3 lbs.                     in 1993; the area was closed from                      officially protected in the late 1970’s
                                                (1.36 kg) for Nassau grouper. This was                  December 1 to March 1 to protect                       and only residents were allowed to fish
                                                followed in 1998 with a 10-day seasonal                 spawning aggregations. A seasonal                      by lines during the spawning season
                                                closure at several spawning                             closure zone to protect Nassau grouper                 (Hill and Sadovy de Mitcheson 2013). In
                                                aggregations. An annual ‘‘two-month’’                   spawning aggregations was included                     1986, increasing complaints from
                                                fishery closure was added in December                   when the Bacalar Chico marine reserve                  fishermen of a decline in both numbers
                                                2003 to coincide with the spawning                      was established in 1996 (Paz and Truly                 and size of Nassau grouper taken from
                                                period and was extended to three                        2007). Minimum and maximum capture                     the fishery prompted the
                                                months in 2005 to encompass the                         sizes were later introduced (Hill and                  implementation of a monitoring
                                                December through February spawning                      Sadovy de Mitcheson 2013 and citations                 program by the Department of the
                                                period. Up until 2015, the                              therein).                                              Environment (Bush et al. 2006).
                                                implementation of the 3-month closure                      In 2001 the Belize National Spawning                   Following the development of the
                                                was determined annually and could be                    Aggregation Working Group established                  monitoring program, the Cayman
                                                shortened or otherwise influenced by                    protective legislation for 11 of the                   Islands implemented a number of
                                                such factors as the economy (Sadovy                     known Nassau grouper spawning sites                    management measures. In the early
                                                and Eklund 1999). In 2015, the annual                   within Belize. Seven of those 11 sites                 1990s, legislation prohibited
                                                assessment of the closure was removed                   are monitored as regularly as possible.                spearfishing at spawning aggregation
                                                ensuring a fixed 3-month closure each                   The Working Group meets regularly to                   sites. In 1998, the three main grouper
                                                year moving forward (Fisheries                          share data and develop management                      holes at the eastern end of the islands
                                                Resources [Jurisdiction and                             strategies (www.spagbelize.org; retrieved              were formally designated as ‘‘Restricted
                                                Conservation] [Amendment]                               on 15 April 2012). In 2003, Belize                     Marine Areas’’ where access requires
                                                Regulations 2015). During the 3-month                   introduced a four-month closed season                  licensing by the Marine Conservation
                                                closure there is a national ban on                      to protect spawning fish (O’Connor                     Board (Bush et al. 2006). In February
                                                Nassau grouper catches; however, the                    2002, Gibson 2008). However, the 2003                  2002, protective legislation defined a
                                                Bahamas Reef Educational Foundation                     legislation also allowed for exemptions                spawning season as November 1 to
                                                (BREEF; unpub. data), has reported large                to the closures by special license                     March 31, and an ‘‘Alternate Year
                                                numbers of fish being taken according to                granted by the Fisheries Administrator,                Fishing’’ rule was passed. This law
                                                fisher accounts with photo-                             provided data be taken on any Nassau                   allowed fishing of the spawning
                                                documentation and confirming reports                    grouper removed. These special licenses                aggregations to occur every other year
                                                of poaching of the species during the                   made it difficult to enforce the national              with the first non-fishing year starting in
                                                aggregation season.                                     prohibition and in 2010 Belize stopped                 2003. A catch limit of 12 Nassau
                                                   The Bahamas has implemented                          issuing permits to fish for Nassau                     grouper per boat, per day during fishing
                                                several other actions that aid the                      grouper during the 4-month spawning                    years was also set. The 2002 law defined
                                                conservation of Nassau grouper. There                   period, except at Maugre Caye and                      a one nautical mile (nm) ‘‘no trapping’’
                                                are marine parks in the Bahamas that                    Northern Two Caye.                                     zone around each spawning site, and set
                                                are closed to fishing year round and                       In 2009, Belize issued additional                   a minimum size limit of 12 inches for
                                                therefore protect Nassau grouper. The                   protective measures to help manage and                 Nassau grouper in response to juveniles
                                                Exuma Cays Land and Sea Park, first                     protect the Nassau grouper. These                      being taken by fish traps inside the
                                                established in 1959, has been closed to                 include minimum and maximum size                       sounds (Whaylen et al. 2004, Bush et al.
                                                fishing since 1986, thus protecting both                limits of 20 inches and 30 inches,                     2006). In 2003, spearguns were
                                                nursery and adult habitat for Nassau                    respectively. Belize has also introduced               restricted from use within 1 nm of any
                                                grouper and other depleted marine                       a plan to ban spear fishing within all                 designated grouper spawning area from
                                                species. Other sites, including the South               marine reserves (yet to be                             November through March. In 2008, it
                                                Berry Islands Marine Reserve                            implemented). Furthermore, as a large                  was prohibited to take any Nassau
                                                (established on December 29, 2008),                     proportion of finfish are landed as                    grouper by speargun anywhere in
                                                Southwest New Providence National                       fillets, the new regulations require that              Cayman waters. Effective December 29,
                                                Park, and North Exumas Study Site have                  all Nassau grouper be landed whole,                    2003, the Marine Conservation Board,
                                                also been established and closed to                     and if filleted must have a 1-inch by 2-               closed fishing at all designated Nassau
                                                fishing. Several gear restrictions in the               inch skin patch (The Belize Spawning                   grouper spawning sites for a period of
                                                Bahamas are also protective of Nassau                   Aggregation Working Group 2009).                       8 years. The conservation measure was
                                                grouper. Fishing with SCUBA and the                     Other gear restrictions are in place to                renewed for a further 8 years in 2011.
                                                use of explosives, poisons, and                         generally aid in the management of reef                   In Cuba, there is a minimum size limit
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                                                spearguns is prohibited in the Bahamas,                 fish, such as no spearfishing on                       for Nassau grouper though this
                                                although snorkeling with sling spears is                compressed air.                                        regulation is largely unprotective. The
                                                allowed. The use of bleach or other                        Although Bermuda closed red hind                    minimum size of 32 cm TL (or 570g) for
                                                noxious or poisonous substances for                     aggregation sites in 1974, Nassau                      Nassau grouper is less than the reported
                                                fishing, or possession of such                          grouper aggregation sites located                      average size at maturity of 50 cm TL,
                                                substances on board a fishing vessel,                   seaward of these sites were not included               indicating that Nassau grouper can be
                                                without written approval of the                         and continued to be fished. In 1990, a                 harvested before having the opportunity


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                                                                 Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations                                          42279

                                                to reproduce. Of some benefit to Nassau                 southwest coast of St. Thomas, U.S.V.I.                the spawning season is not allowed
                                                grouper are more general fishing                        in 1990. This area, known as the Hind                  (Bohnsack 1989, Sadovy and Eklund
                                                regulations such as bag limits for                      Bank Marine Conservation District                      1999, Box and Bonilla Mejia 2008) and
                                                recreational fishing, regulations to                    (HBMCD), was intended to protect red                   at least one marine park has been
                                                increase selectivity of fishing gears to                hind and their spawning aggregations,                  established with fishing regulations. In
                                                avoid the catch of juveniles, limits of                 as well as a former Nassau grouper                     Guadeloupe and Martinique, there are
                                                net use during spawning aggregation                     spawning site (Brown 2007). The                        plans to protect the species (F. Gourdin,
                                                time, and controls of speargun use, both                HBMCD was first subject to a seasonal                  Regional Activity Center for Specially
                                                commercially and recreationally.                        closure beginning in 1990 (Beets and                   Protected Areas and Wildlife—UNEP,
                                                Marine protected areas have also been                   Friedlander 1999, Nemeth 2005,                         pers. comm. to Y. Sadovy, University of
                                                introduced throughout the country. In                   Nemeth et al. 2006) to protect spawning                Hong Kong, 2011) although no details
                                                2002, the total number of recreational                  aggregations of red hind, and was later                are available at this time. In Honduras,
                                                licenses was limited to 3,500 for the                   closed to fishing year-round in 1998                   there is no legislation that controls
                                                whole country hoping to reduce                          (DPNR 2005). Additional fishing                        fishing in the snapper/grouper fishery;
                                                directed fishing pressure nationally.                   restrictions in the U.S.V.I. such as gear              however, traps and spears are illegal in
                                                   In Mexico, following scientific                      restrictions, rules on the sale of fish, and           the Bay Islands. There are no Nassau
                                                documentation of declines of Nassau                     protected areas such as the Virgin                     grouper special regulations in Jamaica;
                                                grouper at Mahahual (Aguilar-Perera                     Islands Coral Reef National Monument                   yet, some marine protected areas were
                                                1994), two regulations were enacted: (1)                and Buck Island Reef National                          designated in 2011.
                                                In 1993 spear-fishing was banned at any                 Monument where all take is prohibited,
                                                spawning aggregation site in southern                                                                          Analysis of Existing Regulatory
                                                                                                        Virgin Islands National Park
                                                Quintana Roo; and (2) in 1997 the                                                                              Mechanisms
                                                                                                        (commercial fishing prohibited), and
                                                fishing of any grouper species was                      several U.S.V.I. marine reserves offer                    The ERAG considered several threats
                                                banned during December and January                      additional protection to Nassau grouper.               under Factor D including law
                                                (Aguilar-Perera 2006). Then, in 2003, a                 In 2006, the U.S.V.I. instituted                       enforcement, international trade
                                                closed season for all grouper was                       regulations to prohibit harvest and                    regulations, foreign regulations in their
                                                implemented from February 15 to                         possession of Nassau grouper in                        jurisdictional waters, U.S. federal laws,
                                                March 15 in all waters of the Mexican                   territorial waters and filleting at sea was            and U.S. state and territorial laws. The
                                                Exclusive Economic Zone. Although                       prohibited (Garcı́a-Moliner and Sadovy                 ERAG determined that these threats
                                                aimed at protecting red grouper this                    2008).                                                 substantially contribute to the overall
                                                closure also protects Nassau grouper                       In Colombia, the San Andrés                        risk to the species. Inadequate law
                                                during a part of its spawning season                    Archipelago has a number of areas that                 enforcement was noted by several ERAG
                                                (Aguilar-Perera et al. 2008). A                         are designated as no-take fishing zones,               members as influencing their scoring for
                                                management plan was to have gone into                   and in 2000 the entire archipelago was                 abundance, fishing of spawning
                                                effect in 2012 to protect all                           declared by the United Nations                         aggregations, commercial harvest, and
                                                commercially exploited groupers in                      Educational, Scientific and Cultural                   historical harvest. Inadequate law
                                                Mexico’s southern Gulf of Mexico and                    Organization (UNESCO) as the                           enforcement led to higher risk scores for
                                                Caribbean Sea; yet at this time the plan                Seaflower Biosphere Reserve. In 2004,                  each of these threats. The ERAG scored
                                                has not been implemented.                               large portions of the archipelago were                 law enforcement as a ‘‘high risk’’ threat
                                                   In the Turks and Caicos Islands, the                 declared as a system of marine protected               for Nassau grouper. ERAG rankings for
                                                only documented Nassau grouper                          areas with varying zones of fisheries                  the other threats were widely
                                                spawning aggregation site is protected                  management; however, enforcement is                    distributed. The inadequacy of foreign
                                                from fishing in Northwest Point Marine                  largely lacking (M. Prada, Coralina, San               regulations in jurisdictional waters was
                                                National Park, Providenciales (DECR                     Andres, Colombia, pers. comm. R. Hill,                 considered an ‘‘increasing’’ risk while
                                                2004; National Parks Ordinance and                      NMFS, 2010). Right-to-fish laws in                     the risk of international trade
                                                Subsidiary Legislation CAP. 80 of 1988).                Colombia also require that fishermen be                regulations was ‘‘unknown.’’ The
                                                Similar to situations in other countries,               allowed to fish at a subsistence level                 remaining two categories of regulations
                                                protection of Nassau grouper habitat                    even within the no-take zones (M.                      (U.S. Federal and State of Florida/U.S.
                                                and spawning migration corridors on                     Prada, Coralina, San Andres, Colombia,                 territory regulations) were considered
                                                the narrow ledge of Caicos Bank is                      pers. comm. R. Hill, NMFS, 2010).                      ‘‘low risk’’ and ‘‘moderate risk’’
                                                problematic as it would impose                             There are other Caribbean countries                 respectively. While the ERAG rankings
                                                economic hardship on local fishers who                  that have either few management                        for threats impacting the adequacy of
                                                depend on those areas for commercial                    measures in place or have yet to                       regulatory mechanisms were generally
                                                species (e.g., spiny lobsters) and                      implement any conservation measures                    moderate, we believe the concern about
                                                subsistence fishing (Rudd 2001).                        for Nassau grouper. We are not aware of                fishing at spawning aggregations (‘‘high
                                                   In U.S. federal waters, including those              special conservation or management                     risk’’ according to the ERAG) is due in
                                                federal waters around Puerto Rico and                   regulations for Nassau grouper in                      part to the inadequacy of existing
                                                the U.S.V.I., take and possession of                    Anguilla. In Antigua-Barbuda, while                    regulatory mechanisms.
                                                Nassau grouper have been prohibited                     Nassau grouper is not specifically                        Overall, we believe existing regulatory
                                                since 1990. Since 1993, a ban on                        managed or protected, closed seasons                   mechanisms throughout the species’
                                                fishing/possessing Nassau grouper was                   were considered in 2008 for Nassau                     range (international trade, foreign, U.S.
                                                implemented for the state of Florida and                grouper and red hind, though the status                federal, and U.S. state and territorial
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                                                has since been enacted in all U.S. state                of these closed seasons is not known. In               regulations) vary in their effectiveness,
                                                waters. The species was fully protected                 the British Virgin Islands, there is a                 especially in addressing the most
                                                in both state and federal waters of                     closed season for landing Nassau                       serious threat to Nassau grouper—
                                                Puerto Rico by 2004. The Caribbean                      grouper between March 1 and May 31                     fishing of spawning aggregations. In
                                                Fishery Management Council, with                        (Munro and Blok 2005). In the                          some countries, an array of national
                                                support of local fishermen, established                 Dominican Republic the catch and sale                  regulatory mechanisms, increases in
                                                a no-take marine protected area off the                 of ripe female Nassau grouper during                   marine protected areas, and customary


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                                                42280            Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations

                                                management may be effective at                          aggregations, while other local                        aquaculture was a ‘‘very low’’ risk threat
                                                addressing fishing of spawning                          circulation patterns may entrain larvae                to Nassau grouper. Experiments to
                                                aggregations. For example, the Exuma                    (Colin et al. 1987) making the                         determine the success rate of larval
                                                Cays Land and Sea Park (Bahamas), has                   population entirely self-recruiting.                   Nassau grouper culture (Watanabe et al.
                                                been closed to fishing for over 25 years                  In conclusion, although many                         1995a, 1995b) and survival of released
                                                and protects both nursery and adult                     countries have taken regulatory                        hatchery-reared juveniles have been
                                                habitat for Nassau grouper and other                    measures to conserve Nassau grouper,                   conducted and feasibility of restocking
                                                marine species. In that park, there is a                the species faces an ongoing threat due                reefs has been tested (Roberts et al.
                                                clear difference in the number, biomass,                to the inadequacy of regulatory                        1995) in St. Thomas, U.S.V.I. However,
                                                and size of Nassau grouper in                           mechanisms to prevent or remediate the                 the potential of Nassau grouper stock
                                                comparison to adjacent areas where                      impacts of other threats that are                      enhancement, as with any other grouper
                                                fishing is permitted (Sluka et al. 1997).               elevating the species’ extinction risk,                species, has yet to be determined
                                                   We note, however, that many                          particularly fishing of spawning                       (Roberts et al. 1995). Serious concerns
                                                countries have few, if any, specific                    aggregations.                                          about the genetic consequences of
                                                Nassau grouper regulations. Instead they                                                                       introducing Nassau grouper raised in
                                                                                                        E. Other Natural or Manmade Factors
                                                rely on general fisheries regulations                                                                          facilities, possible problems of juvenile
                                                                                                        Affecting Its Continued Existence
                                                (e.g., Anguilla, Antigua-Barbuda,                                                                              habitat availability, introduction of
                                                Colombia, and Cuba all rely only on size                   The ERAG considered climate change                  maladapted individuals, and the
                                                limits, while Guadeloupe and                            as a threat to Nassau grouper including                inability of stocked individuals to locate
                                                Martinique, Honduras, Jamaica, Mexico,                  global warming, sea level rise, and                    traditional spawning locations, continue
                                                St. Lucia, and the Turks and Caicos rely                ocean acidification for Factor E.                      to be raised. Given the number of
                                                on a variety of general fishing                         Although Nassau grouper occur across a                 concerns with aquaculture and the fact
                                                regulations). Additionally, where                       range of temperatures, spawning occurs                 that some spawning aggregations
                                                Nassau grouper-specific regulations do                  when sea surface temperatures range                    remain, we believe that it is unlikely
                                                exist, the ERAG scores indicated that                   between 25 °C–26 °C (Colin 1992,                       that Nassau grouper aquaculture will
                                                law enforcement still presents a high                   Tucker and Woodward 1996). Because                     develop further. Therefore we agree
                                                risk threat to the species. We agree with               Nassau grouper spawn in a narrow                       with the ERAG that aquaculture
                                                the ERAG’s risk assessment and believe                  window of temperatures, a rise in sea                  presents a very low extinction risk to
                                                that law enforcement in many foreign                    surface temperature outside that range                 Nassau grouper and is not contributing
                                                countries is less than adequate, thus                   could impact spawning or shift the                     to the species’ current status.
                                                rendering the regulations ineffective.                  geographic range of it to overlap with                    Demographic factors of abundance,
                                                   Some foreign regulations may be                      waters within the required temperature                 population growth rate/productivity and
                                                ephemeral, unprotective of migrating                    parameters. Increased sea surface                      diversity were also considered by the
                                                adults, or inadequate to conserve the                   temperatures have also been linked to                  ERAG under Factor E. Each ERAG
                                                viability of a species. In some cases,                  coral loss through bleaching and                       member considered whether the species
                                                regulations do not completely protect all               disease. Further, increased global                     is likely to be able to maintain a
                                                known spawning aggregations (e.g.,                      temperatures are also predicted to                     sustainable population size and
                                                Belize, where 2 spawning aggregations                   change parasite-host relationships and                 adequate genetic diversity. They also
                                                are fished by license). In another                      may present additional unknown                         considered whether the species is at risk
                                                instance, we found no protections for                   concerns (Harvell et al. 2002,                         due to a loss in the breeding population,
                                                Nassau grouper in any foreign country                   Marcogliese 2001). Rising sea surface                  which leads to a reduction in survival
                                                during the period they move to and                      temperatures are also associated with                  and production of eggs and offspring.
                                                from spawning aggregation sites.                        sea level rise. If sea level changed                   Trends or shifts in demographic or
                                                Foreign regulations in some countries                   rapidly, water depth at reef sites may be              reproductive traits were considered
                                                specify exemptions for ‘‘historical,’’                  modified with such rapidity that coral                 when assessing the ranking of threats by
                                                ‘‘local,’’ or artisanal fishermen (e.g.,                and coral reefs could be affected                      each ERAG member to identify a decline
                                                Colombia). Finally, some particular                     (Munday et al. 2008).                                  in population growth rate. The ERAG
                                                types of regulations are insufficient to                   Another potential effect of climate                 scores indicated that abundance of
                                                protect the species (e.g., minimum size                 change could be the loss of structural                 Nassau grouper was a ‘‘moderate risk,’’
                                                limits in both the Bahamas and Cuba are                 habitat in coral reef ecosystems as ocean              growth rate/productivity was an
                                                less than size-at-maturity).                            acidification is anticipated to affect the             ‘‘increasing risk,’’ and that diversity was
                                                   In some places, such as Bermuda, no                  integrity of coral reefs (Munday et al.                a ‘‘moderate risk.’’ We agree with these
                                                recovery has been documented after                      2008). Bioerosion may reduce the 3-                    rankings and believe they are supported
                                                years of regulations (B. Luckhurst,                     dimensional structure of coral reefs                   by the declining number and size of
                                                Bermuda Department of Agriculture,                      (Alvarez-Filip et al. 2009), reducing                  spawning aggregations, which affects
                                                Fisheries, and Parks, pers. comm. to Y.                 adult habitat for Nassau grouper                       growth rate/productivity and diversity.
                                                Sadovy, University of Hong Kong,                        (Coleman and Koenig 2010, Rogers and
                                                September, 2012). In other places (e.g.,                Beets 2001). Results of the ERAG scores                NMFS’s Conclusions From Threats
                                                Cayman Islands) there are indications of                indicated that climate change was an                   Evaluation
                                                potential recovery at spawning                          ‘‘unknown risk’’ to Nassau grouper. We                   The most serious threats to Nassau
                                                aggregation sites, but fishing continues                agree with the assessment of the ERAG                  grouper are fishing at spawning
                                                to keep the population depressed                        and believe there is not enough                        aggregations and inadequate law
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                                                (Semmens et al. 2012) and inconsistent                  information at this time to determine                  enforcement. These threats, considered
                                                surveys do not provide data adequate to                 how climate change is affecting the                    under Factors B and D, were rated by
                                                realize impacts. Additionally, larval                   extinction risk of Nassau grouper now                  the ERAG as ‘‘high risk’’ threats to the
                                                recruitment is highly variable due to                   or in the foreseeable future.                          species. We agree with the ERAG’s
                                                currents in the Caribbean basin. Some                      The ERAG also considered threats                    assessment that these threats are
                                                populations may receive larval input                    from aquaculture to Nassau grouper                     currently affecting the status of Nassau
                                                from neighboring spawning                               under Factor E and determined that                     grouper, putting it at a heightened risk


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                                                                 Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations                                           42281

                                                of extinction. A variety of other threats                  Abundance is closely related with the               adversely affecting the status of Nassau
                                                were identified by the ERAG as also                     other three demographic factors. Growth                grouper as discussed above, but disagree
                                                impacting the status of this species.                   rate/productivity, spatial structure and               with the ERAG’s ranking of historic
                                                Growth rate/productivity (Factor E),                    connectivity, and diversity are all                    harvest as a high risk. These high risk
                                                spatial structure/connectivity (Factors A               negatively affected by decreased                       threats will continue to elevate the
                                                and E), and effectiveness of foreign                    abundance associated with                              extinction risk of Nassau grouper over
                                                regulations (Factor D) were identified by               overexploitation. Historical overfishing               the foreseeable future. Both threats
                                                the ERAG as ‘‘increasing risks.’’                       has led to a decreased average length                  directly affect the current abundance of
                                                Artificial selection (Factor B),                        and earlier age at maturity in exploited               the species, its ability to maintain
                                                abundance (Factors B and E), diversity                  populations, which affects the species’                population growth rate, the population
                                                (Factor E), commercial harvest (Factors                 ability to maintain the population                     structure of the species, and its diversity
                                                B and D), and effectiveness of state and                growth rate above replacement level.                   in terms of genetics and overall ecology.
                                                territory regulations (Factor D) were                   Reductions in the number and                              As previously described, the ERAG
                                                determined to be ‘‘moderate risks.’’                    distribution of spawning aggregations                  analyzed inadequate law enforcement as
                                                NMFS concurs that these threats have                    has the potential to affect larval and                 a standalone threat under Factor D,
                                                the potential to adversely affect the                   juvenile dispersal. This can further                   inadequacy of existing regulatory
                                                status of Nassau grouper over the                       affect genetic diversity within the                    mechanisms, and ranked it as a ‘‘high
                                                foreseeable future.                                     population. However, we don’t believe                  risk’’ threat. We agree that existing
                                                                                                        that any of these demographic factors                  regulations, and enforcement of existing
                                                Extinction Risk Analysis                                                                                       regulations, are inadequate to control
                                                                                                        have been adversely affected to the
                                                   We must assess the ERA results and                   point that Nassau grouper is currently in              the threat posed by fishing on spawning
                                                make a determination as to whether the                  danger of extinction. As described                     aggregations, and thus this threat under
                                                Nassau grouper is currently in danger of                previously, the species continues to                   Factor D is contributing to the
                                                extinction, or likely to become so within               occupy its current range, spawning is                  extinction risk and status of Nassau
                                                the foreseeable future. We first                        still occurring in several locations thus              grouper.
                                                evaluated the current status of the                     continuing to deliver new recruits to the                 Based on the information in the
                                                Nassau grouper in light of the four                     population, and recovery of spawning                   Biological Report and the results from
                                                demographic factors. Based on our                       aggregations has been documented in                    the ERA, we conclude that ESA Factors
                                                assessment of the ERA in regards to                     locations with adequate regulatory                     B (overutilization for commercial,
                                                these demographic factors (abundance,                   mechanisms and enforcement. The size                   recreational, scientific, or educational
                                                growth rate/productivity, spatial                       of Nassau grouper is also increasing in                purposes), D (inadequacy of regulatory
                                                structure and connectivity, and                         areas where protections are in place                   mechanisms), and E (other natural or
                                                diversity) we do not believe the Nassau                 (e.g., Belize and U.S.V.I.), indicating                manmade factors) are contributing to a
                                                grouper is currently in danger of                       that current abundance is not adversely                threatened status for Nassau grouper.
                                                extinction. Each of these demographic                   affecting growth rate and productivity at              Overutilization in the form of historical
                                                factors was ranked by the ERAG as a                     these locations.                                       harvest has reduced population size and
                                                moderate or increasing risk to the                         After considering the current status of             led to the collapse of spawning
                                                species’ current status.                                Nassau grouper based on the four                       aggregations in many locations. While
                                                   We acknowledge that the abundance                    demographic factors, we next assessed                  some countries have made efforts to
                                                of Nassau grouper has been dramatically                 how the identified threats are expected                curb harvest, fishing at spawning
                                                reduced in relation to historical records,              to affect the status of the species,                   aggregation sites remains a ‘‘high risk’’
                                                but we do not believe abundance is                      including its demographic factors, over                threat. Further contributing to the risk of
                                                currently so low that the species is at                 the foreseeable future. The ERAG                       Nassau grouper extinction is the
                                                risk of extinction from stochastic events,              identified a variety of threats that have              inadequacy of regulatory control and
                                                environmental variation, anthropogenic                  the potential to impact Nassau grouper.                law enforcement, which leads to
                                                perturbations, lack of genetic diversity,               The ERAG ranked and we agreed that                     continued overutilization (low
                                                or depensatory processes. Although the                  several threats (habitat alteration,                   abundance), reduced reproductive
                                                reduced abundance of Nassau grouper                     disease, aquaculture, and U.S. federal                 output, and reduced recruitment. If
                                                has diminished the size and number of                   regulations) ranked as ‘‘very low’’ or                 growth and sexual recruitment rates
                                                spawning aggregations, spawning is still                ‘‘low’’ risk, will have little to no effect            cannot balance the loss from these
                                                occurring and abundance is increasing                   on the extinction risk of Nassau grouper               threats, populations will become more
                                                in some locations (e.g. Cayman Islands                  within the foreseeable future. Several                 vulnerable to extinction over the future
                                                and Bermuda) where adequate                             other threats (commercial harvest,                     (Primack 1993).
                                                protections are effectively being                       artificial selection, foreign regulations
                                                implemented. The abundance of Nassau                                                                           Protective Efforts
                                                                                                        within jurisdictional waters, and
                                                grouper is now patchily distributed                     regulations of the U.S. and its                           Section 4(b)(1)(A) of the ESA requires
                                                throughout the Caribbean with areas of                  territories), were ranked as moderate or               the Secretary, when making a listing
                                                higher abundance correlated with those                  increasing risks to the status of Nassau               determination for a species, to take into
                                                areas with effective regulations. We                    grouper. We agree that collectively these              consideration those efforts, if any, being
                                                believe the abundance of Nassau                         threats could cause Nassau grouper to                  made by any State or foreign nation to
                                                grouper in these protected areas is large               become in danger of extinction within                  protect the species. To evaluate the
                                                enough to sustain the overall population                the foreseeable future.                                efficacy of domestic efforts that have not
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                                                and limit extinction risk. However, we                     Finally, the ERAG identified three                  yet implemented or that have been
                                                also believe that further regulations will              threats that present a ‘‘high’’ risk to the            implemented, but have not yet
                                                be necessary in other countries to                      status of Nassau grouper over the                      demonstrated to be effective, the
                                                counteract past population declines and                 foreseeable future. We agree with the                  Services developed a joint ‘‘Policy for
                                                ultimately recover the population of                    ERAG’s assessment that fishing of                      Evaluation of Conservation Efforts
                                                Nassau grouper throughout the                           spawning aggregations combined with                    When Making Listing Decisions’’
                                                Caribbean.                                              inadequate law enforcement is currently                (‘‘PECE’’; 68 FR 15100; March 28, 2003).


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                                                42282            Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations

                                                The PECE is designed to ensure                          and Guadeloupe and Martinique’s plans                  would be in danger of extinction, or
                                                consistent and adequate evaluation on                   to protect the species. Because these                  likely to become so in the foreseeable
                                                whether domestic conservation efforts                   proposed plans are several years old                   future, throughout all of its range.’’
                                                that have been recently adopted or                      with no updates or known                               Thus, if the species is found to be
                                                implemented, but not yet proven to be                   implementation, we find that there is                  threatened or endangered throughout its
                                                successful, will result in recovering the               not a sufficient basis to conclude that                range, we do not separately evaluate
                                                species to the point at which listing is                there is a reasonable certainty of                     portions of the species’ range.
                                                not warranted or contribute to forming                  implementation or effectiveness. We                       Although the SPOIR Policy had yet to
                                                the basis for listing a species as                      also considered the marine protected                   go into effect during our status review
                                                threatened rather than endangered. The                  areas implemented by Jamaica in 2011,                  of Nassau grouper, we considered the
                                                PECE is expected to facilitate the                      though based on Jamaica’s historic                     interpretations and principles contained
                                                development of conservation efforts by                  overfishing and difficulty in enforcing                in the 2014 Draft Policy with regards to
                                                states and other entities that sufficiently             existing regulations, we find that there               the Nassau grouper and completed an
                                                improve a species’ status so as to make                 is not a sufficient basis to conclude that             assessment of potential ‘‘SPOIR,’’ which
                                                listing the species as threatened or                    these marine protected areas present a                 is documented in the ERA. However,
                                                endangered unnecessary.                                 reasonable certainty of effectiveness in               throughout the status review process
                                                   The PECE establishes two overarching                 reducing threats that contribute to                    NMFS determined threats and risks to
                                                criteria to use in evaluating efforts                   Nassau grouper’s extinction risk. We                   the status of Nassau grouper are
                                                identified in conservations plans,                      carefully considered the other                         affecting the species over the entirety of
                                                conservation agreements, management                     conservation efforts summarized in the                 its range. Because the threats and risks
                                                plans or similar documents: (1) The                     Biological Report and acknowledge that                 are widespread throughout the entire
                                                certainty that the conservation efforts                 time is required to see the benefit of                 range of this species, there is no portion
                                                will be implemented; and (2) the                        mature adults in the spawning                          of the range that can be considered
                                                certainty that the efforts will be                      aggregations; however, the continued                   ‘‘significant.’’
                                                effective. While section 4(b)(1)(A)                     decline in number and size of Nassau                   Listing Determination
                                                requires that we evaluate both domestic                 grouper spawning aggregations indicates
                                                and foreign conservation efforts, it does               the effectiveness of those conservation                  Based on the Biological Report, the
                                                not set out particular criteria for doing               efforts is currently unknown and thus                  Threats Evaluation, the Extinction Risk
                                                so. While the particular framework of                   there is insufficient basis to conclude                Analysis, and Protective Efforts we
                                                the PECE policy only directly applies to                there is a reasonable certainty of                     determined that the Nassau grouper
                                                consideration of domestic efforts, we                   effectiveness. While some conservation                 warrants a threatened status under the
                                                have discretion to evaluate foreign                     efforts have been partially successful on              ESA. We summarize the results of our
                                                efforts using a similar approach and find               localized scales, Nassau grouper appear                comprehensive status review as follows:
                                                that it is reasonable to do so here. In our             to still be overutilized and at heightened             (1) The species is made up of a single
                                                discretion, we evaluated foreign                        risk of extinction based on the ERA.                   population over a broad geographic
                                                conservation efforts to protect and                     After taking into account these                        range, and its current range is
                                                recover Nassau grouper that are either                  conservation efforts, our evaluation of                indistinguishable from its historical
                                                underway, but not yet fully                             the section 4(a)(1) factors is that the                range; (2) the species possesses life
                                                implemented, or are only planned,                       conservation efforts do not reduce the                 history characteristics that increase
                                                using these overarching criteria.                       risk of extinction of Nassau grouper to                vulnerability to unregulated harvest; (3)
                                                   Conservation efforts with the                        the point at which listing is not                      historical harvest greatly diminished the
                                                potential to address identified threats to              warranted.                                             population of Nassau grouper and the
                                                Nassau grouper include, but are not                                                                            species has yet to recover from this
                                                limited to, fisheries management plans,                 Significant Portion of Range                           overexploitation; (4) spawning
                                                education about overfishing and fishing                    There are two situations under which                aggregations have drastically declined
                                                of spawning aggregations, and projects                  a species is eligible for listing under                in size and number across the species’
                                                addressing the health of coral reef                     ESA: A species may be endangered or                    range; (5) there are two threats the
                                                ecosystems. These conservation efforts                  threatened throughout all of its range or              ERAG rated as ‘‘high risk,’’ that we agree
                                                may be conducted by countries, states,                  a species may be endangered or                         are affecting the current status of the
                                                local governments, individuals, NGOs,                   threatened throughout only a                           species and will continue to do so over
                                                academic institutions, private                          ‘‘significant portion of its range’’                   the foreseeable future—fishing at
                                                companies, individuals, or other                        (SPOIR). Although the ESA does not                     spawning aggregations and inadequate
                                                entities. They also include global                      define ‘‘SPOIR,’’ NMFS and the U.S.                    law enforcement; and (6) historical
                                                conservation organizations that conduct                 Fish and Wildlife Service (USFWS)                      harvest has abated, though existing
                                                coral reef and/or marine environment                    published a final policy clarifying their              regulatory mechanisms and law
                                                conservation projects, global coral reef                interpretation of this phrase (79 FR                   enforcement have not been effective in
                                                monitoring networks and research                        37577; July 7, 2014). Under the policy,                preventing fishing at many spawning
                                                projects, regional or global conventions,               if a species is found to be endangered                 aggregation sites. Conservation efforts in
                                                and education and outreach projects                     or threatened throughout only a                        some nations (U.S., Puerto Rico,
                                                throughout the range of Nassau grouper.                 significant portion of its range, the                  U.S.V.I., and Belize) have almost
                                                   The Biological Report summarizes                     entire species is subject to listing and               certainly prevented further declines.
                                                known conservation efforts, including                   must be protected everywhere. A                        Given the life history characteristics of
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                                                those that have yet to be fully                         portion of a species’ range is                         Nassau grouper, more time will be
                                                implemented or have yet to demonstrate                  ‘‘significant’’ if ‘‘. . . the species is not          needed to determine if these protective
                                                effectiveness. Conservation efforts that                currently endangered or threatened                     measures are successful in recovering
                                                we considered that are yet to be fully                  throughout its range, but the portion’s                the population. Collectively, the
                                                implemented include Mexico’s 2012                       contribution to the viability of the                   information obtained during the status
                                                proposed management plan, Antigua-                      species is so important that, without the              review indicates the species is not
                                                Barbuda’s 2008 closed season proposal,                  members in that portion, the species                   currently in danger of extinction


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                                                                 Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations                                          42283

                                                (though reduced in number, the species                  management considerations or                           pursuant to ESA section 4(d), we will
                                                maintains its historical range and still                protection; and (2) specific areas outside             evaluate whether there are protective
                                                forms spawning aggregations at some                     the geographical area occupied by a                    regulations we deem necessary and
                                                sites), but it is likely to become                      species at the time it is listed upon a                advisable for the conservation of Nassau
                                                endangered within the foreseeable                       determination that such areas are                      grouper, including application of some
                                                future (based on continued risk of                      essential for the conservation of the                  or all of the take prohibitions. If
                                                harvest, especially at spawning                         species. ‘‘Conservation’’ means the use                protective regulations are deemed
                                                aggregation sites inadequately                          of all methods and procedures needed                   necessary, a proposed 4(d) rule would
                                                controlled by regulations and law                       to bring the species to the point at                   be subject to public comment.
                                                enforcement). Accordingly, we have                      which listing under the ESA is no
                                                                                                                                                               Policies on Peer Review
                                                determined that the Nassau grouper                      longer necessary. Critical habitat may
                                                warrants listing as a threatened species                also include areas unoccupied by                         In December 2004, the Office of
                                                under the ESA.                                          Nassau grouper if those areas are                      Management and Budget (OMB) issued
                                                                                                        essential to the conservation of the                   a Final Information Quality Bulletin for
                                                Effects of Listing                                                                                             Peer Review establishing minimum peer
                                                                                                        species.
                                                  Conservation measures provided for                       Section 4(a)(3)(A) of the ESA (16                   review standards, a transparent process
                                                species listed as endangered or                         U.S.C. 1533(a)(3)(A)) requires that, to                for public disclosure of peer review
                                                threatened under the ESA include                        the maximum extent prudent and                         planning, and opportunities for public
                                                recovery plans (16 U.S.C. 1533(f)),                     determinable, critical habitat be                      participation. The OMB Bulletin,
                                                critical habitat designations (16 U.S.C.                designated concurrently with the listing               implemented under the Information
                                                1533(a)(3)(A)), Federal agency                          of a species. Pursuant to 50 CFR                       Quality Act (Pub. L. 106–554) is
                                                consultation requirements (16 U.S.C.                    424.12(a), designation of critical habitat             intended to enhance the quality and
                                                1536), and protective regulations (16                   is not determinable when one or both of                credibility of the Federal government’s
                                                U.S.C. 1533(d)). Recognition of the                     the following situations exist: Data                   scientific information, and applies to
                                                species’ status through listing promotes                sufficient to perform required analyses                influential or highly influential
                                                conservation actions by Federal and                     are lacking; or the biological needs of                scientific information disseminated on
                                                state agencies, private groups, and                     the species are not sufficiently well                  or after June 16, 2005. To satisfy our
                                                individuals, as well as the international               known to identify any area that meets                  requirements under the OMB Bulletin,
                                                community. Both a recovery program                      the definition of ‘‘critical habitat.’’                we obtained independent peer review of
                                                and designation of critical habitat could               Although we have gathered information                  the Biological Report. Five independent
                                                result from this final listing. Given its               through the status review and public                   specialists were selected from the
                                                broad range across the Caribbean Sea, a                 comment periods on the habitats                        academic and scientific community,
                                                regional cooperative effort to protect                  occupied by this species, we currently                 Federal and state agencies, and the
                                                and restore Nassau grouper is necessary.                do not have enough information to                      private sector for this review (with three
                                                We anticipate that protective regulations               determine what physical and biological                 respondents). All peer reviewer
                                                for Nassau grouper will also be                         features within those habitats facilitate              comments were addressed prior to
                                                necessary for the conservation of the                   the species’ life history strategy and are             dissemination of the final Biological
                                                species. Federal, state, and the private                thus essential to the conservation of                  Report and publication of this final rule.
                                                sectors will need to cooperate to                       Nassau grouper, and may require special                Solicitation of Information
                                                conserve listed Nassau grouper and the                  management considerations or
                                                ecosystems upon which they depend.                      protection. To the maximum extent                        We are soliciting information on
                                                                                                        prudent and determinable, we will                      features and areas that may support
                                                Identifying ESA Section 7 Consultation                  publish a proposed designation of                      designation of critical habitat for Nassau
                                                Requirements                                            critical habitat for Nassau grouper in a               grouper. Information provided should
                                                   Section 7(a)(2) of the ESA and NMFS/                 separate rule. Designations of critical                identify the physical and biological
                                                FWS regulations require Federal                         habitat must be based on the best                      features essential to the conservation of
                                                agencies to consult with us on any                      scientific data available and must take                the species and areas that contain these
                                                actions they authorize, fund, or carry                  into consideration the economic,                       features. Areas outside the occupied
                                                out if those actions may affect the listed              national security, and other relevant                  geographical area should also be
                                                species or designated critical habitat.                 impacts of specifying any particular area              identified if such areas themselves are
                                                Based on currently available                            as critical habitat. Once critical habitat             essential to the conservation of the
                                                information, we can conclude that                       is designated, section 7 of the ESA                    species. Essential features may include,
                                                examples of Federal actions that may                    requires Federal agencies to ensure that               but are not limited to, features specific
                                                affect Nassau grouper include, but are                  they do not fund, authorize, or carry out              to the species’ range, habitats, and life
                                                not limited to, artificial reef creation,               any actions that are likely to destroy or              history characteristics within the
                                                dredging, pile-driving, military                        adversely modify that habitat. This                    following general categories of habitat
                                                activities, and fisheries management                    requirement is in addition to the section              features: (1) Space for individual growth
                                                practices.                                              7 requirement that Federal agencies                    and for normal behavior; (2) food, water,
                                                                                                        ensure that their actions do not                       air, light, minerals, or other nutritional
                                                Critical Habitat                                                                                               or physiological requirements; (3) cover
                                                                                                        jeopardize the continued existence of
                                                   Critical habitat is defined in section 3             listed species.                                        or shelter; (4) sites for reproduction and
                                                of the ESA (16 U.S.C. 1532(5)) as: (1)                                                                         development of offspring; and (5)
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                                                The specific areas within the                           Identification of Those Activities That                habitats that are protected from
                                                geographical area occupied by a species,                Would Constitute a Violation of Section                disturbance or are representative of the
                                                at the time it is listed in accordance                  9 of the ESA                                           historical, geographical, and ecological
                                                with the ESA, on which are found those                    Because we are proposing to list                     distributions of the species (50 CFR
                                                physical or biological features (a)                     Nassau grouper as threatened, the ESA                  424.12(b)). ESA implementing
                                                essential to the conservation of the                    section 9 prohibitions do not                          regulations at 50 CFR 424.12(h) specify
                                                species and (b) that may require special                automatically apply. Therefore,                        that critical habitat shall not be


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                                                42284            Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations

                                                designated within foreign countries or                   Environmental Policy Act (See NOAA                         disproportionate effect on minority and
                                                in other areas outside of U.S.                           Administrative Order 216–6).                               low-income communities. This final
                                                jurisdiction. Therefore, we request                                                                                 rule is not expected to have a
                                                                                                         Executive Order 12866, Regulatory
                                                information only on potential areas of                                                                              disproportionately high effect on
                                                                                                         Flexibility Act and Paperwork
                                                critical habitat within waters in U.S.                   Reduction Act                                              minority populations or low-income
                                                jurisdiction.                                                                                                       populations.
                                                   For features and areas potentially                       As noted in the Conference Report on
                                                qualifying as critical habitat, we also                  the 1982 amendments to the ESA,                            List of Subjects in 50 CFR Part 223
                                                request information describing: (1)                      economic impacts cannot be considered                        Endangered and threatened species,
                                                Activities or other threats to the                       when assessing the status of a species.                    Exports, Transportation.
                                                essential features or activities that could              Therefore, the economic analysis
                                                                                                         requirements of the Regulatory                               Dated: June 21, 2016.
                                                be affected by designating them as
                                                                                                         Flexibility Act are not applicable to the                  Samuel D Rauch, III,
                                                critical habitat, and (2) the positive and
                                                negative economic, national security                     listing process. In addition, this final                   Deputy Assistant Administrator for
                                                                                                         rule is exempt from review under                           Regulatory Programs, National Marine
                                                and other relevant impacts, including
                                                                                                         Executive Order 12866. This final rule                     Fisheries Service.
                                                benefits to the recovery of the species,
                                                likely to result if these areas are                      does not contain a collection-of-                            For the reasons set out in the
                                                designated as critical habitat.                          information requirement for the                            preamble, we amend 50 CFR part 223 as
                                                                                                         purposes of the Paperwork Reduction                        follows:
                                                References                                               Act.
                                                  A complete list of the references used                                                                            PART 223—THREATENED MARINE
                                                                                                         Executive Order 13132, Federalism
                                                in this final rule is available at: (http://                                                                        AND ANADROMOUS SPECIES
                                                sero.nmfs.noaa.gov/protected_                               In keeping with the intent of the
                                                resources/listing_petitions/species_esa_                 Administration and Congress to provide                     ■ 1. The authority citation for part 223
                                                consideration/index.html).                               continuing and meaningful dialogue on                      continues to read as follows:
                                                                                                         issues of mutual state and Federal
                                                Classifications                                                                                                        Authority: 16 U.S.C. 1531–1543; subpart B,
                                                                                                         interest, the proposed rule was provided                   § 223.201–202 also issued under 16 U.S.C.
                                                National Environmental Policy Act                        to the relevant agencies in each state in                  1361 et seq.; 16 U.S.C. 5503(d) for
                                                                                                         which the subject species occurs, and                      § 223.206(d)(9).
                                                  The 1982 amendments to the ESA, in                     these agencies were invited to comment.
                                                section 4(b)(1)(A), restrict the                         We did not receive comments from any                       ■ 2. In § 223.102, amend the table in
                                                information that may be considered                       state agencies.                                            paragraph (e) by adding an entry under
                                                when assessing species for listing. Based                                                                           the ‘‘Fishes’’ subheading for ‘‘Grouper,
                                                on this limitation of criteria for a listing             Executive Order 12898, Environmental                       Nassau’’ in alphabetical order to read as
                                                decision and the opinion in Pacific                      Justice                                                    follows:
                                                Legal Foundation v. Andrus, 675 F. 2d                      Executive Order 12898 requires that
                                                825 (6th Cir. 1981), NMFS has                            Federal actions address environmental                      § 223.102 Enumeration of threatened
                                                concluded that ESA listing actions are                   justice in the decision-making process.                    marine and anadromous species.
                                                not subject to the environmental                         In particular, the environmental effects                   *       *    *       *        *
                                                assessment requirements of the National                  of the actions should not have a                               (e) * * *

                                                                                      Species 1
                                                                                                                                          Citation(s) for listing determination(s)   Critical habitat   ESA rules
                                                                                                           Description of listed
                                                    Common name                 Scientific name                   entity


                                                         *                        *                        *                          *                       *                      *                   *
                                                        FISHES

                                                         *                      *                         *                         *                  *                             *                   *
                                                Grouper, Nassau .......    Epinephelus striatus ..       Entire species ............ [Insert Federal Register citation],                     NA              NA
                                                                                                                                        June 29, 2016.

                                                          *                       *                        *                          *                       *                      *                   *
                                                   1 Speciesincludes 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).
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                                                                 Federal Register / Vol. 81, No. 125 / Wednesday, June 29, 2016 / Rules and Regulations                                          42285

                                                *      *     *       *      *                           can be found in the preamble of the                    November 2015, for Amendment 9 to
                                                [FR Doc. 2016–15101 Filed 6–28–16; 8:45 am]             proposed rule published on May 2, 2013                 the 2006 Consolidated Atlantic Highly
                                                BILLING CODE 3510–22–P                                  (78 FR 25685). Copies are available from               Migratory Species Fishery Management
                                                                                                        NMFS (see ADDRESSES), or can be                        Plan (November 24, 2015; 80 FR 73128).
                                                                                                        viewed electronically at the Federal E-                That final rule, among other things,
                                                DEPARTMENT OF COMMERCE                                  Rulemaking portal for this action: http://             allows for the at-sea removal of smooth
                                                                                                        www.regulations.gov.                                   dogfish fins provided that fishing occurs
                                                National Oceanic and Atmospheric                                                                               within 50 nautical miles of shore along
                                                Administration                                          II. Major Components of the Final
                                                                                                                                                               the Atlantic Coast from Maine through
                                                                                                        Action
                                                                                                                                                               the east coast of Florida; smooth dogfish
                                                50 CFR Part 600                                            Retaining a shark fin while discarding              fin weight does not exceed 12 percent
                                                                                                        the shark carcass (shark finning) has                  of the carcass weight on board; smooth
                                                [Docket No. 111014628–6513–02]
                                                                                                        been prohibited in the United States                   dogfish make up at least 25 percent of
                                                RIN 0648–BB54                                           since the 2000 Shark Finning                           the total retained catch, by weight; and
                                                                                                        Prohibition Act. The 2010 SCA included                 the fisherman/vessel holds both federal
                                                Magnuson-Stevens Fishery                                provisions that amended the Magnuson-                  and state permits appropriate for the
                                                Conservation and Management Act                         Stevens Fishery Conservation and                       retention of smooth dogfish.
                                                Provisions; Implementation of the                       Management Act (MSA) to prohibit any                      This final rule also combines the
                                                Shark Conservation Act of 2010                          person from: (1) Removing any of the                   existing §§ 600.1203 and 600.1204 into
                                                AGENCY:  National Marine Fisheries                      fins of a shark (including the tail) at sea;           one section. The text throughout 50 CFR
                                                Service (NMFS), National Oceanic and                    (2) having custody, control, or                        part 600, subpart N, is amended to make
                                                Atmospheric Administration (NOAA),                      possession of a fin aboard a fishing                   it consistent with the provisions of the
                                                Commerce.                                               vessel unless it is naturally attached to              SCA.
                                                                                                        the corresponding carcass; (3)                            The MSA authorizes the Secretary to
                                                ACTION: Final rule.
                                                                                                        transferring a fin from one vessel to                  regulate fisheries seaward of the inner
                                                SUMMARY:   This final action updates                    another vessel at sea, or receiving a fin              boundary of the U.S. exclusive
                                                agency regulations consistent with                      in such transfer, unless the fin is                    economic zone (EEZ), which is defined
                                                provisions of the Shark Conservation                    naturally attached to the corresponding                as a line coterminous with the seaward
                                                Act of 2010 (SCA) and prohibits any                     carcass; or (4) landing a fin that is not              boundary of each U.S. coastal state. 16
                                                person from removing any of the fins of                 naturally attached to the corresponding                U.S.C. 1802(11). Thus, as noted in the
                                                a shark at sea, possessing shark fins on                carcass, or landing a shark carcass                    proposed rule, the SCA provisions
                                                board a fishing vessel unless they are                  without its fins naturally attached. For               apply to any person subject to the
                                                naturally attached to the corresponding                 the purpose of the SCA and these                       jurisdiction of the United States,
                                                carcass, transferring or receiving fins                 regulations, ‘‘naturally attached,’’ with              including persons on board U.S. and
                                                from one vessel to another at sea unless                respect to a shark fin, means to be                    foreign vessels, engaging in activities
                                                the fins are naturally attached to the                  attached to the corresponding shark                    prohibited under the statute with
                                                corresponding carcass, landing shark                    carcass through some portion of uncut                  respect to sharks harvested seaward of
                                                fins unless they are naturally attached to              skin.                                                  the inner boundary of the EEZ. See 78
                                                the corresponding carcass, or landing                      This action amends NMFS’                            FR 25685, 25686 (May 2, 2013). Federal
                                                                                                        regulations consistent with these                      regulations pertaining to the
                                                shark carcasses without their fins
                                                                                                        provisions of the SCA. Specifically, the               conservation and management of
                                                naturally attached. This action amends
                                                                                                        rule amends regulations at 50 CFR part                 specific shark fisheries are set forth in
                                                existing regulations and makes them
                                                                                                        600, subpart N, to prohibit the removal                parts 635, 648, and 660 of title 50 of the
                                                consistent with the SCA.
                                                                                                        of shark fins at sea, namely, the                      Code of Federal Regulations. For
                                                DATES: Effective July 29, 2016.                         possession, transfer and landing of                    Atlantic highly migratory species
                                                ADDRESSES: Copies of the                                shark fins that are not naturally attached             fisheries, as a condition of its Federal
                                                Environmental Assessment (EA)/                          to the corresponding carcass, and the                  permit, a vessel’s fishing, catch, and
                                                Regulatory Impact Review (RIR)/Final                    landing of shark carcasses without the                 gear are subject to federal requirements
                                                Regulatory Flexibility Analysis (FRFA)                  corresponding fins naturally attached.                 even when fishing in state waters. See
                                                prepared for this action can be obtained                In the preamble to the proposed rule,                  50 CFR 635.4(a)(10) (noting also that,
                                                from: Erin Wilkinson, National Marine                   NMFS noted that it interprets the                      when fishing within the waters of a state
                                                Fisheries Service, 1315 East-West                       prohibitions in subpart N as applying to               with more restrictive regulations,
                                                Highway, Room 13437, Silver Spring                      sharks, not skates and rays, and                       persons aboard the vessel must comply
                                                MD 20910. An electronic copy of the                     solicited public comment on whether                    with those requirements). This rule
                                                EA/RIR/FRFA document as well as                         clarification was needed in the                        amends 50 CFR part 600, subpart N, and
                                                copies of public comments received can                  regulatory text on this issue. See 78 FR               does not supersede or amend any other
                                                be viewed at the Federal e-rulemaking                   25685, 25686 (May 2, 2013). NMFS                       federal regulation or requirement related
                                                portal: http://www.regulations.gov/                     received only one public comment on                    to the conservation and management of
                                                (Docket ID: NOAA–NMFS–2012–0092).                       this point, which was supportive of this               sharks.
                                                FOR FURTHER INFORMATION CONTACT: Erin                   interpretation, and NMFS thus affirms                     The SCA also amended the High Seas
                                                Wilkinson by phone at 301–427–8561,                     in this final rule that the prohibitions do            Driftnet Fishing Moratorium Protection
                                                or by email: erin.wilkinson@noaa.gov or                 not apply to skates and rays.                          Act, which provides for identification
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                                                sca.rulemaking@noaa.gov.                                   This final rule also updates subpart N              and certification of nations to address
                                                SUPPLEMENTARY INFORMATION:                              to be consistent with section 103(b) of                illegal, unreported, or unregulated
                                                                                                        the SCA regarding an exception for                     fishing; bycatch of protected living
                                                I. Overview of the Shark Conservation                   individuals engaged in commercial                      marine resources; and, as amended by
                                                Act                                                     fishing for smooth dogfish.                            the SCA, shark catches. 16 U.S.C.
                                                   Background information and an                        Interpretation of that exception was                   1826h–1826k. With regard to sharks, the
                                                overview of the Shark Conservation Act                  addressed in a rule finalized in                       High Seas Driftnet Fishing Moratorium


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Document Created: 2018-02-08 07:42:43
Document Modified: 2018-02-08 07:42:43
CategoryRegulatory Information
CollectionFederal Register
sudoc ClassAE 2.7:
GS 4.107:
AE 2.106:
PublisherOffice of the Federal Register, National Archives and Records Administration
SectionRules and Regulations
ActionFinal rule; request for information.
DatesThe effective date of this final rule is July 29, 2016. Information on features, areas, and potential impacts, that may support designation of critical habitat for Nassau grouper must be received by August 29, 2016.
ContactAdam Brame, NMFS, Southeast Regional Office (727) 209-5958; or Lisa Manning, NMFS, Office of Protected Resources (301) 427-8466.
FR Citation81 FR 42268 
RIN Number0648-XA98
CFR AssociatedEndangered and Threatened Species; Exports and Transportation

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