80_FR_57498 80 FR 57314 - Endangered and Threatened Wildlife and Plants: Proposed Threatened Status for Island Grouper (Mycteroperca fusca) and Endangered Status for Gulf Grouper (Mycteroperca jordani) Under the Endangered Species Act (ESA)

80 FR 57314 - Endangered and Threatened Wildlife and Plants: Proposed Threatened Status for Island Grouper (Mycteroperca fusca) and Endangered Status for Gulf Grouper (Mycteroperca jordani) Under the Endangered Species Act (ESA)

DEPARTMENT OF COMMERCE
National Oceanic and Atmospheric Administration

Federal Register Volume 80, Issue 184 (September 23, 2015)

Page Range57314-57331
FR Document2015-23502

We, NMFS, announce 12-month findings and listing determinations on a petition to list the gulf grouper (Mycteroperca jordani) and the island grouper (Mycteroperca fusca) as threatened or endangered under the Endangered Species Act (ESA). We have completed comprehensive status reviews for these two marine fish species in response to a petition submitted by WildEarth Guardians. After reviewing the best scientific and commercial data available, we have determined that the gulf grouper is currently in danger of extinction throughout its range and, therefore, meets the definition of an endangered species. After reviewing the best scientific and commercial data available, we have also determined that the island 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. Therefore, we conclude that the island grouper meets the definition of a threatened species. We are soliciting information that may be relevant to inform the final determinations for these two species.

Federal Register, Volume 80 Issue 184 (Wednesday, September 23, 2015)
[Federal Register Volume 80, Number 184 (Wednesday, September 23, 2015)]
[Proposed Rules]
[Pages 57314-57331]
From the Federal Register Online  [www.thefederalregister.org]
[FR Doc No: 2015-23502]


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DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

50 CFR Parts 223 and 224

[Docket No. 150527481-5834-01]
RIN 0648-XD971


Endangered and Threatened Wildlife and Plants: Proposed 
Threatened Status for Island Grouper (Mycteroperca fusca) and 
Endangered Status for Gulf Grouper (Mycteroperca jordani) Under the 
Endangered Species Act (ESA)

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

ACTION: Proposed rule; 12-month findings; request for comments.

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SUMMARY: We, NMFS, announce 12-month findings and listing 
determinations on a petition to list the gulf grouper (Mycteroperca 
jordani) and the island grouper (Mycteroperca fusca) as threatened or 
endangered under the Endangered Species Act (ESA). We have completed 
comprehensive status reviews for these two marine fish species in 
response to a petition submitted by WildEarth Guardians. After 
reviewing the best scientific and commercial data available, we have 
determined that the gulf grouper is currently in danger of extinction 
throughout its range and, therefore, meets the definition of an 
endangered species. After reviewing the best scientific and commercial 
data available, we have also determined that the island 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. Therefore, we conclude that the island grouper meets the 
definition of a threatened species. We are soliciting information that 
may be relevant to inform the final determinations for these two 
species.

DATES: Comments on this proposed rule must be received by November 23, 
2015. Public hearing requests must be made by November 9, 2015.

ADDRESSES: You may submit comments on this document, identified by the 
code NOAA-NMFS-2015-0071, by either of the following methods:
     Electronic Submission: Submit all electronic public 
comments via the Federal eRulemaking Portal. Go to www.regulations.gov/#!docketDetail;D=NOAA-NMFS-2015-0071. Click the ``Comment Now'' icon, 
complete the required fields. Enter or attach your comments.
     Mail: Submit written comments to, Ron Salz, NMFS Office of 
Protected Resources (F/PR3), 1315 East West Highway, Silver Spring, MD 
20910, USA.
    Instructions: Comments sent by any other method, to any other 
address or individual, or received after the end of the comment period, 
may not be considered. All comments received are a part of the public 
record and will generally be posted for public viewing on http://www.regulations.gov without change. All personal identifying 
information (e.g., name, address, etc.), confidential business 
information, or otherwise sensitive information submitted voluntarily 
by the sender will be publicly accessible. We will accept anonymous 
comments (enter ``N/A'' in the required fields if you wish to remain 
anonymous). Attachments to electronic comments will be accepted in 
Microsoft Word, Excel, or Adobe PDF file formats only.
    You can obtain the petition, status review reports, proposed rule, 
and list of references electronically on our NMFS Web site at http://www.nmfs.noaa.gov/pr/species/petition81.htm.

FOR FURTHER INFORMATION CONTACT: Ronald Salz, NMFS, Office of Protected 
Resources (OPR), (301) 427-8171 or Marta Nammack, NMFS, OPR, (301) 427-
8403.

SUPPLEMENTARY INFORMATION:

Background

    On July 15, 2013, we received a petition from WildEarth Guardians 
to list 81 marine species or subpopulations as threatened or endangered 
under the Endangered Species Act (ESA). This petition included species 
from many different taxonomic groups, and we prepared our 90-day 
findings in batches by taxonomic group. We found that the petitioned 
actions may be warranted for 24 of the species and 3 of the 
subpopulations and announced the initiation of status reviews for each 
of the 24 species and 3 subpopulations (78 FR 63941, October 25, 2013; 
78 FR 66675, November 6, 2013; 78 FR 69376, November 19, 2013; 79 FR 
9880, February 21, 2014; and 79 FR 10104, February 24, 2014). This 
document addresses the 12-month findings for two of these species: Gulf 
grouper (Mycteroperca jordani) and island grouper (Mycteroperca fusca). 
The status of the findings and relevant Federal Register notices for 
the other 21 species and 3 subpopulations can be found on our Web site 
at http://www.nmfs.noaa.gov/pr/species/petition81.htm.
    We are responsible for determining whether species are threatened 
or endangered under the ESA (16 U.S.C. 1531 et seq.). To make this 
determination, we consider first whether a group of organisms 
constitutes a ``species'' under the ESA, then whether the status of the 
species qualifies it for listing as either threatened or endangered. 
Section 3 of the ESA defines a ``species'' to include ``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.'' On February 7, 1996, NMFS and the U.S. Fish and Wildlife 
Service (USFWS; together, the Services) adopted a policy describing 
what constitutes a distinct population segment (DPS) of a taxonomic 
species (the DPS Policy; 61 FR 4722). The DPS Policy identified two 
elements that must be considered when identifying a DPS: (1) The 
discreteness of the population segment in relation to the remainder of 
the species (or subspecies) to which it belongs; and (2) the 
significance of the population segment to the remainder of the species 
(or subspecies) to which it belongs. As stated in the DPS Policy, 
Congress expressed its expectation that the Services would exercise 
authority with regard to DPSs sparingly and only when the biological 
evidence indicates such action is warranted. Based on the scientific 
information available, we determined that the gulf grouper 
(Mycteroperca jordani) and the island grouper (Mycteroperca fusca) are 
both ``species'' under the ESA. There is nothing in the scientific 
literature indicating that either of these species should be further 
divided into subspecies or DPSs.
    Section 3 of the ESA defines an endangered species as ``any species 
which is in danger of extinction throughout all or a significant 
portion of its range'' and a threatened species as one ``which is 
likely to become an endangered species within the foreseeable future 
throughout all or a significant portion of its range.'' We interpret an 
``endangered species'' to be one that is presently in danger of 
extinction. A ``threatened species,'' on

[[Page 57315]]

the other hand, is not presently in danger of extinction, but is likely 
to become so in the foreseeable future (that is, at a later time). In 
other words, the primary statutory difference between a threatened and 
endangered species is the timing of when a species may be in danger of 
extinction, either presently (endangered) or in the foreseeable future 
(threatened).
    When we consider whether a species might qualify as threatened 
under the ESA, we must consider the meaning of the term ``foreseeable 
future.'' It is appropriate to interpret ``foreseeable future'' as the 
horizon over which predictions about the conservation status of the 
species can be reasonably relied upon. The foreseeable future considers 
the life history of the species, habitat characteristics, availability 
of data, particular threats, ability to predict threats, and the 
reliability to forecast the effects of these threats and future events 
on the status of the species under consideration. Because a species may 
be susceptible to a variety of threats for which different data are 
available, or which operate across different time scales, the 
foreseeable future is not necessarily reducible to a particular number 
of years.
    Section 4(a)(1) of the ESA requires us to determine whether any 
species is endangered or threatened due to any one or a combination of 
the following five threat factors: The present or threatened 
destruction, modification, or curtailment of its habitat or range; 
overutilization for commercial, recreational, scientific, or 
educational purposes; disease or predation; the inadequacy of existing 
regulatory mechanisms; or other natural or manmade factors affecting 
its continued existence. We are also required to make listing 
determinations based solely on the best scientific and commercial data 
available, after conducting a review of the species' status and after 
taking into account efforts being made by any state or foreign nation 
to protect the species.
    In assessing extinction risk of these two species, we considered 
the demographic viability factors developed by McElhany et al. (2000) 
and the risk matrix approach developed by Wainwright and Kope (1999) to 
organize and summarize extinction risk considerations. The approach of 
considering demographic risk factors to help frame the consideration of 
extinction risk has been used in many of our status reviews (see http://www.nmfs.noaa.gov/pr/species for links to these reviews). In this 
approach, the collective condition of individual populations is 
considered at the species level according to four demographic viability 
factors: Abundance, growth rate/productivity, spatial structure/
connectivity, and diversity. These viability factors reflect concepts 
that are well-founded in conservation biology and that individually and 
collectively provide strong indicators of extinction risk.
    Scientific conclusions about the overall risk of extinction faced 
by the gulf grouper and the island grouper under present conditions and 
in the foreseeable future are based on our evaluation of the species' 
demographic risks and section 4(a)(1) threat factors. Our assessment of 
overall extinction risk considered the likelihood and contribution of 
each particular factor, synergies among contributing factors, and the 
cumulative impact of all demographic risks and threats on the species.
    We then assess efforts being made to protect the species, to 
determine if these conservation efforts are adequate to mitigate the 
existing threats. 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, or any political subdivision of a State or foreign nation, to 
protect the species.
    Status reviews for the gulf grouper and the island grouper were 
conducted by NMFS OPR staff and an in-house contractor. In order to 
complete the status reviews, we compiled the best available information 
on the species' biology, ecology, life history, threats, and 
conservation status from information contained in the petition, our 
files, a comprehensive literature search, and consultation with 
experts. We also considered information submitted by the public in 
response to our petition findings. Draft status review reports were 
also submitted to independent peer reviewers; comments and information 
received from peer reviewers were addressed and incorporated as 
appropriate before finalizing the draft reports. The gulf grouper and 
island grouper status review reports are available on our Web site (see 
ADDRESSES section). Below we summarize information from these reports 
and the status of each species.

Status Reviews

Gulf Grouper

    The following section describes our analysis of the status of the 
gulf grouper, Mycteroperca jordani.
Species Description
    The gulf grouper (Jenkins and Evermann 1889) is a large, heavy-
bodied grouper with rounded preopercle and moderate sized scales (Smith 
1971). They have a comparatively elongated and compressed body shape 
with body depth much less than their head length (Jenkins and Evermann 
1889, Heemstra and Randall 1993). The dorsal fin has 11 spines and 16 
to 17 rays, with the posterior margin rounded (Heemstra and Randall 
1993). The anal fin has 3 spines and 10 to 11 rays; and the gill rakers 
range from 21 to 26, not counting rudiments (Heemstra and Randall 
1993). Juvenile gulf grouper are greyish-brown with large, dark grey 
oblong blotches on the dorsal part of the body and fins (Heemstra and 
Randall 1993). Female adults are generally dark brown to grey, but they 
can assume a juvenile pattern when disturbed or excited. Larger adult 
males develop a white margin along the pectoral fin, with the medial 
fin developing a narrow white edge (Heemstra and Randall 1993). In 
spawning aggregations, breeding individuals exhibit conspicuous dark 
lines radiating from the eye (Sala et al. 2003). Gulf grouper can grow 
up to 150 cm (in total length), 91 kg (in weight), and 48 years 
(Heemstra and Randall 1993, Aburto-Oropeza et al. 2008). Gulf grouper 
are considered voracious, solitary predators, though little is known 
about their diet or feeding behavior.
Reproductive Biology and Spawning Behavior
    Gulf grouper are a protogynous hermaphroditic fish, meaning they 
mature as females and, later in life, transition into males. Gulf 
grouper mature as females at an estimated six to seven years of age 
(Aburto-Oropeza et al. 2008). Gulf grouper are believed to transition 
from female to male based upon their size (size-advantage model) 
(Bhandari et al. 2006, Zhou and Gui 2010). The size-advantage model 
theorizes that if it is advantageous for one sex to reproduce at a 
small size and the other sex to reproduce at a larger size, then the 
individual should change sex at some point in life (Ghiselin 1969, 
Bhandari et al. 2006). Larger female grouper produce substantially more 
and higher quality eggs than smaller females. Although not studied 
directly in gulf grouper, an eight-year-old female Mycteroperca 
produces approximately 60 times the number of eggs that a five-year-old 
female produces (Aburto-Oropeza et al. 2008). For males, larger size is 
advantageous when competing with other males for reproduction 
opportunities with females at spawning aggregation sites (Domeier and 
Colin 1997).

[[Page 57316]]

    Gulf grouper are transient aggregate spawners. Domeier and Colin 
(1997) defined spawning aggregations as ``a group of conspecific fish 
gathered for the purpose of spawning, with fish densities or numbers 
significantly higher than those found in the area of aggregation during 
the non-reproductive periods.'' Spawning aggregations are further 
categorized as either ``resident'' or ``transient'' depending upon 
aggregation criteria. Transient spawning aggregations typically (1) 
draw individuals from a relatively large area (individuals travel days 
to weeks to gather), (2) occur during a very specific time of year (one 
or two months), (3) persist for only a few-day period, and (4) do not 
occur year-round (Domeier and Colin 1997). Transient aggregate species 
are often large sized predators that are not known to spawn outside of 
aggregations (Domeier and Colin 1997).
    The location and timing of gulf grouper spawning aggregations may 
depend upon tidal influences on egg or larvae distribution (Domeier and 
Colin 1997, Cherubin et al. 2011). All known spawning aggregation sites 
for gulf grouper, current and historical, are found in the Gulf of 
California (GOC) (Sala et al. 2004, S[aacute]enz-Arroyo et al. 2005a, 
Moreno-Baez 2010). The GOC, with its length and combinations of basins, 
islands, and sills, has large tides (up to 4 m) and fast tidal currents 
(up to 1.5 m/sec) which peak during the full moon (Filonov and 
Lav[iacute]n 2003). Gulf grouper are found on predictable spawning 
aggregation locations before and during the full moon in May (Sala et 
al. 2004). Their spawning aggregation sites consist of rocky reef 
(gorgonians and black coral) seamounts with abrupt relief habitat at 20 
to 35 m depths. Adult gulf grouper form spawning aggregations of 40 or 
more individuals in areas larger than 1,000 m\2\ (Aburto-Oropeza et al. 
2008). Based upon three observed spawning aggregations, gulf grouper 
spawning aggregation density was estimated at 220 fish/ha with fish 
sizes ranging from 100 to 150 cm total length (Sala et al. 2003). Along 
the Pacific coast, spawning aggregation sites for gulf groupers are an 
unknown, though the size of the historical gulf grouper fisheries 
suggests that spawning aggregation sites may have been present.
Population Structure, Distribution, Abundance and Habitat
    The gulf grouper resides in the subtropical eastern Pacific Ocean 
and Gulf of California from 32.84[deg] N. (La Jolla, California, United 
States) to 23.22[deg] N. (Mazatl[aacute]n, Sinaloa, Mexico) (Heemstra 
and Randall 1993). The overall range distribution for gulf grouper is 
considered restricted, defined as less than 800,000 km\2\ (Morris et 
al. 2000). Gulf grouper habitat requirements vary throughout life. 
Groupers in general pass through a pelagic larvae phase (20-50 days) 
during which they settle into rocky, coastal reefs (Aburto-Oropeza et 
al. 2008). After this phase, they acquire juvenile characteristics 
while they settle into shallow, coastal habitats (e.g. Sargassum beds, 
seagrass areas, mangroves, and estuaries); this nursery stage can last 
up to two years. Adult gulf grouper predominately use rocky reefs and 
kelp beds of depths from five to 30 meters (Heemstra and Randall 1993) 
and deeper (30 to 45 m) during the summer (Moreno-Ba[eacute]z 2010). 
During the spawning season, gulf grouper will aggregate in rocky reefs 
in depths from 20 to 35 m (Sala et al. 2003).
    Historical and current gulf grouper population abundance is 
unknown. Estimated trends in gulf grouper abundance are based primarily 
on limited fisheries catch data and anecdotal reports. The available 
information indicates that gulf grouper were once a dominant species in 
rocky-reef fish communities in terms of biomass, before stocks 
collapsed in the early 1970s (S[aacute]enz-Arroyo et al. 2005a). In the 
1930s, California fishermen reported gulf grouper as being abundant in 
Mexican waters between Bah[iacute]a Tortugas and Bah[iacute]a 
Magdalena, and this species represented an important component of the 
commercial fishery south of the U.S.-Mexico border (Croaker 1937, Fitch 
1949). Combined landings of gulf grouper and broomtail grouper for the 
California commercial fishery peaked in the early 1950s at 376 metric 
tons (mt), declined to around 100-150 mt between the late 1950s until 
the late 1960s, after which the grouper fishery completely crashed to 
near zero landings by 1970 (California Department of Fish and 
Wildlife--http://libraries.ucsd.edu/apps/ceo/fishbull/). In 1976, the 
California Department of Fish and Game adopted no-take prohibitions for 
broomtail grouper and gulf grouper that are still in effect today.
    In the GOC, gulf grouper accounted for a significant proportion of 
the commercial landings weight in the mid-20th century. In 1960, gulf 
grouper represented approximately 45 percent of the artisanal fishery 
in the GOC (Aburto-Oropeza et al. 2008). Based on anecdotal accounts, 
boats from El Club de Vuelos sport fishing resort in Loreto (Mexico) 
landed an estimated 63 mt of gulf grouper during a 2-month period in 
1962 (S[aacute]enz-Arroyo et al. 2005a). By comparison, only an 
estimated 58 mt of gulf grouper were harvested from 2006 through 2012 
throughout the species' entire range. The El Club de Vuelos boats 
fished at the Punta Lobos and San Bruno seamounts, both probable 
spawning aggregation sites at that time. There are also anecdotal 
reports from the 1940s and 1950s of fishermen using dynamite to capture 
large numbers of gulf grouper at the San Bruno seamount (S[aacute]enz-
Arroyo et al. 2005a). S[aacute]enz-Arroyo et al. (2005a) conducted over 
30 dives from 2001 through 2004 during the gulf grouper spawning season 
at sites that were recommended by the original fishermen from El Club 
de Vuelos. During these dives, only three gulf grouper were observed, 
all at the Punta Lobos seamount. In 2002 and 2003, a biologist fished 
the San Bruno seamount during the spawning aggregation season and was 
only able to capture one gulf grouper (S[aacute]enz-Arroyo et al. 
2005a). Since official Mexican fishery landings data at the species 
level are only available since 2007, these data fail to encapsulate the 
major decline in GOC gulf grouper abundance, which likely started in 
the mid-20th century.
Summary of Factors Affecting the Gulf Grouper
    Available information regarding current, historical, and potential 
future threats to the gulf grouper was thoroughly reviewed (Dennis 
2015). We summarize information regarding threats below according to 
three (out of five) factors specified in section 4(a)(1) of the ESA: 
``Present or Threatened Destruction, Modification, or Curtailment of 
its Habitat or Range''; ``Overutilization for Commercial, Recreational, 
Scientific, or Educational Purposes''; and ``Inadequacy of Existing 
Regulatory Mechanisms.'' We found very little information regarding 
potential threats that fall into the section 4(a)(1) categories of 
either ``Disease and Predation'' or ``Other Natural or Manmade 
Factors.'' These subjects are data poor, but there are no serious or 
known concerns raised under these threat categories with respect to 
gulf grouper extinction risk; therefore, we do not discuss these 
categories further here. See Dennis (2015) for additional discussion of 
all ESA section 4(a)(1) threat categories.
Present or Threatened Destruction, Modification, or Curtailment of Its 
Habitat or Range
    Since the beginning of the 20th century, human population growth 
and development has resulted in the loss and degradation of coastal 
habitats throughout the gulf grouper's range. Continued loss or 
degradation of these habitats represents a potential threat to

[[Page 57317]]

the species. The terrestrial habitat surrounding the GOC is mostly arid 
to semi-arid with rivers feeding the estuaries and marine waters with 
sediments and fresh water. Originating in these dry environments, the 
rivers and estuaries are of limited supply and great importance. There 
are ten major rivers that provide freshwater, sediment, and nutrient 
inputs to the GOC. These rivers have been extensively dammed, exploited 
for agricultural uses, and polluted from agricultural and urban runoff. 
As a result, the coastal habitats bordering the GOC have been reduced 
and degraded, while nearshore salinities, which ecosystems have evolved 
for, have changed. The R[iacute]o Colorado is the largest watershed 
flowing into the GOC, representing over two-thirds of the GOC's 
watershed acreage. Historically, 16.4 million acre-feet of water flowed 
annually into the GOC from the R[iacute]o Colorado (Goodfriend and 
Flessa 1997, Bureau of Reclamation 2012). Today the river rarely flows 
to the GOC due to the cumulative effects of two large dam projects 
(Hoover Dam and Glen Canyon Dam) and major water diversions. Increased 
anthropogenic nitrogen from sewage, agricultural, and shrimp farming 
sources are directly utilized by macroalgae, creating more frequent 
blooms and corresponding anoxia throughout coastal habitats in the GOC 
(Pi[ntilde][oacute]n-Gimate et al. 2009). Juvenile gulf grouper reside 
in these coastal habitats (such as Sargassum and seagrass beds, 
mangroves, and other kinds of estuary habitats) during the first few 
years of life, and are susceptible to these environmental changes 
(Aburto-Oropeza et al. 2008).
    Shrimp aquaculture began in the GOC in the early 1980s. The 
production of cultivated shrimp in the GOC has increased tremendously 
over the past 30 years: 35 mt in 1985; 15,867 mt in 1995; 33,480 mt in 
2000; and 125,609 mt in 2009 (Gillett 2008, SEPESCA-BC Web page http://www.sepescabc.gob.mx/x/estadisticas/). Shrimp farms can negatively 
impact gulf grouper through direct loss of habitat and through habitat 
degradation. The conversion of natural saltmarshes and mangrove forests 
into shrimp farms can result in the direct loss of nursery areas for 
juvenile gulf grouper (P[aacute]ez-Osuna 2001). In the northern GOC, an 
estimated 95 percent of mangrove forests are impacted by shrimp farms 
(Glenn et al. 2006). GOC shrimp ponds stock between 60,000 to 200,000 
shrimp per hectare, and require a daily water exchange of three to six 
percent (P[aacute]ez-Osuna et al. 1998, P[aacute]ez-Osuna et al. 2003). 
During water exchanges, organic matter from unconsumed shrimp food, 
detritus, phytoplankton, zooplankton, and bacteria is flushed into the 
GOC through discharge channels (Barraza-Guardado et al. 2013). Shrimp 
farm effluents contribute 10.2 percent of the nitrogen and 3.3 percent 
of the phosphorus inputs into the GOC (Miranda et al. 2009). Adding 
these organic materials into the marine habitat, which is already 
receiving effluents from other anthropogenic sources, deteriorates 
water quality through oxygen depletion, light reduction, increased 
salinity, increased chlorophyll and bacteria levels, and changes in 
benthic macrofauna, resulting in possible eutrophication (P[aacute]ez-
Osuna 2001, Barraza-Guardado et al. 2013). For example, the Altata-
Ensenada del Pabell[oacute]n lagoon receives effluent from shrimp 
farms, intensive agriculture (i.e., sugar cane), and sewage from local 
cities, leading to phytoplankton blooms, anoxia, and fish kill events 
(P[aacute]ez-Osuna 1999). The combined effects of shrimp farm effluents 
(and other sources of anthropogenic nutrient loading) with climate 
change may result in an increased incidence of hypoxia due to enhanced 
ocean stratification, decreased oxygen solubility, increased 
metabolism, and increased production of organic matter (Rabalais et al. 
2009). Shrimp farm effluents also typically contain antibiotics which 
are used in large quantities to preemptively treat bacterial diseases 
(Kautsky et al. 2000).
    Effluents from agricultural areas and aquaculture facilities also 
contribute to harmful algal blooms in the GOC. Red tides, which are 
produced by a planktonic dinoflagellate (Prorocentrum minimum), were 
first reported in the GOC in 1990. Between 1990 and 2003, 13 red tide 
events occurred, with six occurring in shrimp ponds and seven occurring 
near aquaculture and agricultural areas (Sierra-Beltr[aacute]n et al. 
2005). Most recently, a red tide occurred in January 2015 near San 
Felipe, Baja California that resulted in fish, bird, and marine mammal 
mortalities.
    GOC reefs are predominantly rocky, with a coral component in the 
south, which shifts to kelp (brown algae) in the north (Squires 1959). 
Reef habitats support a wide diversity and high density of marine life, 
including gulf grouper, and are particularly sensitive to anthropogenic 
threats. Both direct (e.g., fishing with dynamite, dredging) and 
indirect (e.g., anthropogenic nutrients, climate change) activities 
have had a detrimental impact on the reefs within the gulf grouper's 
range. In the past, dynamite was often used for fishing on reefs, which 
has resulted in permanent damage to gulf grouper spawning habitat 
(Lozano-Montes et al. 2008). Development of the GOC region has resulted 
in more dredging activities (Zamora-Arroyo et al. 2005) and increased 
nutrient loading into the marine ecosystem, resulting in algal growth 
and hypoxic waters that can degrade and kill coral (Kline et al. 2006). 
The effects of climate change can lead to coral loss and degradation 
through bleaching and mortality events from elevated ocean 
temperatures, loss of structural integrity, and ocean acidification. 
During the 1997-1998 El Ni[ntilde]o event, sea surface temperature 
anomalies of greater than 1.5 [deg]C occurred from July 1997 through 
January 1998. Coral bleaching was extensive throughout the southern 
GOC: Over 30 percent of live coral cover was bleached, of which, nearly 
70 percent died within a few months (Bonilla 2001). Though the 1997-
1998 coral bleaching event was related to El Ni[ntilde]o, similar 
impacts may be expected in the future due to increasing ocean 
temperatures associated with climate change.
    The impact of anthropogenic activities on GOC marine habitats will 
likely increase in the future based on projected human population 
growth and development in this region. Population growth in the GOC 
region is expected to continue at a high rate with approximately 
150,000 new residents per year (Source: http://www.conapo.gob.mx/es/CONAPO/Proyecciones_Datos). The Mexican federal government has placed a 
major emphasis on tourism and trade development throughout the GOC. 
Beginning in 2008, the first paved highway along the Sonoran GOC coast 
was constructed from Puerto Pe[ntilde]asco to Mexicali (population 
689,775) (Wilder et al. 2012b). In Puerto Pe[ntilde]asco, the 
construction of a new marina with associated breakwaters and facilities 
for cruise liners has started and is expected to be completed in 2015. 
With improved accessibility by land and sea, Puerto Pe[ntilde]asco is 
currently undergoing a construction boom, with two major resorts adding 
over 100,000 rooms via hotels and condominiums along with golf courses 
and 22 small-scale desalination plants (Wilder et al. 2012b). Two 
hundred kilometers south in Puerto Libertad, the Liberty Cove resort 
has been approved for 60,000 dwellings, golf courses, a race track, and 
a marina. Another project, the Escalera N[aacute]utica del Mar de 
Cort[eacute]s y Riviera Maya, will construct 29 new marinas throughout 
the GOC with facilities to accommodate cruise ships and 60,000 boats 
annually (Wilder et al. 2012b).

[[Page 57318]]

Another purpose of the improved ports is to increase trade. For 
example, after dredging its harbor in 2013, the Port of Guaymas became 
the second largest Mexican port and is capable of handling vessels up 
to 130,000 tons, while increasing its port capacity from 8 to 30 
million tons of cargo.
    Increased development and infrastructure will result in increased 
energy and water needs. To meet these needs there are plans to greatly 
expand tidal power and desalination plant capacity in the region. The 
GOC is considered one of the best tidal power locations in the world 
due to its large tides and proximity to urban areas. Two GOC tidal 
power site locations have been identified and are in the early stages 
of planning: Bah[iacute]a de Adair and Canal del Infiernillo. 
Environmental impacts from tidal power include habitat loss, increased 
turbidity, mobilization of contaminants, and changes in the 
morphodynamics of the seabed (Gill 2005, Neill et al. 2009). Plans for 
expanding tourism in the GOC often include construction of desalination 
plants (Wilder et al. 2012b). Desalination plants impact the 
environment by both their very substantial power requirements and the 
wastewater discharges, which include brine plumes (at twice the 
salinity of marine waters), antiscalents, coagulants, heavy metals, and 
membrane preservatives that get released into the marine environment 
(Roberts et al. 2010). Marine organisms can also get trapped in 
desalination intake systems (Wilder et al. 2012a). All of this 
increased development in and around the GOC is anticipated to have 
negative effects on the GOC environment as a whole, and thus, on gulf 
grouper habitat within that environment.
Overutilization for Commercial, Recreational, Scientific, or 
Educational Purposes
    Gulf grouper are a highly prized commercial and recreational fish 
species due to their large size and palatability. Gulf grouper also 
exhibit the following life history traits and behavioral 
characteristics that increase the species' vulnerability to fishery 
overutilization: Slow growth, late maturation, large size, protogynous 
hermaphroditism, long life-span, and the formation of transient 
spawning aggregations (Sadovy 1994). In protogynous hermaphrodites, the 
largest individuals are, in order, terminal males, individuals 
undergoing sexual transition, and the largest, most fecund females who 
are next in line for sexual transition. Since fishers selectively 
harvest the largest individuals, these groups are removed at a high 
rate, leading to decreased productivity of a population. In one study 
of the artisanal fishery of Bah[iacute]a de Los Angeles, nearly 99 
percent of gulf grouper landed from 2002-2003 were immature fish 
(Aburto-Oropeza et al. 2008). These data suggest that large, mature 
gulf grouper have been mostly removed from the population.
    Spawning aggregations sites are particularly vulnerable to 
overfishing because they occur at predictable places and times and they 
contain fish at a much higher than normal density (Domeier and Colin 
1997). Many fishermen base their fishing activities upon the movement 
patterns of target species, and knowledge of spawning aggregation sites 
is highly advantageous (Sadovy et al. 1994, Moreno-B[aacute]ez et al. 
2012). Gulf grouper spawning aggregation sites within the GOC (e.g. 
Punta Lobos and San Bruno seamounts) have disappeared after periods of 
heavy exploitation (S[aacute]enz-Arroyo et al. 2005a). The reduction or 
complete loss of additional spawning aggregations due to overfishing 
represents a continued threat to the gulf grouper.
    Commercial landings of gulf grouper from the Pacific Ocean (U.S. 
vessels fishing in Mexican waters) peaked in the early 1950s, followed 
by a population decline to near commercial extinction by 1970. In 1976, 
California declared the gulf grouper a prohibited species. Based on 
recent fishery independent surveys and fisheries data, the gulf grouper 
is still considered a very rare occurrence in the Pacific Ocean.
    Time series fisheries catch and effort data available for gulf 
grouper in the GOC are sparse. Official Mexican fisheries statistics 
did not include artisanal landings until 1988 (only commercial were 
included prior to that date), and species level information specific to 
gulf grouper are only available since 2007. Currently, gulf grouper 
represent less than one percent of the artisanal fishery in the GOC. 
However, recent gulf grouper landings can be misinterpreted, leading 
one to incorrectly conclude that the gulf grouper is a naturally rare 
species. Anecdotal information based on Local Fishermen Knowledge (LFK) 
indicates that gulf grouper were once abundant in the GOC and 
represented approximately 45 percent of the artisanal fishery landings 
weight in 1960 (S[aacute]enz-Arroyo et al. 2005a). Studies of LFK in 
the GOC indicate sharp declines in gulf grouper abundance over the past 
50 years (Sala et al. 2004, S[aacute]enz-Arroyo et al. 2005a and 2005b, 
Lozano-Montes et al. 2008, and Moreno-B[aacute]ez et al. 2010 and 
2012). S[aacute]enz-Arroyo et al. (2005a and 2005b) interviewed 108 
fishermen from 11 fishing communities in the central GOC. Fishermen 
were asked to recall their best day's catch of gulf grouper, heaviest 
fish caught, and years of these catches. For best day's catch, catches 
decreased significantly over time: 25 fish daily in the 1940s and 
1950s; 10-12 fish daily in the 1960s; and 1-2 fish daily in the 1990s. 
For heaviest gulf grouper caught, weight per fish decreased 
significantly from >= 80 kg from the 1940s through the 1960s to 60 kg 
by 2000. Among age groups, 96 percent of the oldest (>= 55 years old) 
and 90 percent of the middle-aged (31-54 years old) fishermen had 
captured gulf grouper, while only 45 percent of the young fishermen 
(15-30 years old) had. When asked whether or not they considered the 
gulf grouper depleted, 85 percent of the oldest considered them 
depleted, compared to 56 percent of the middle-aged, and 10 percent of 
the young fishermen (S[aacute]enz-Arroyo et al. 2005a and 2005b). Sala 
et al. (2004) interviewed 63 fishermen (ages 25 to 67) from four 
fishing villages along the southern GOC. They found that the relative 
importance of gulf grouper as a target species and the maximum size of 
gulf grouper caught both declined markedly from the 1970s to 2000.
    Gulf grouper are highly prized by recreational anglers, although 
data from this fishery sector are sparse and the impact of recreational 
fishing on this species is largely unknown. Based on anecdotal 
information, recreational anglers caught large numbers of gulf grouper 
in the 1950s and 1960s and likely targeted known spawning aggregation 
sites in the GOC (S[aacute]enz-Arroyo et al. 2005a). During a two-month 
period in 1962, anglers from El Club de Vuelos sport fishing resort 
harvested an estimated 63 mt of gulf grouper (S[aacute]enz-Arroyo et 
al. 2005a). More recently, Cudney-Bueno et al. (2009) reported finding 
a large sport fishing derby targeting gulf grouper in 2004 within the 
no-take zone of the Reserva de la Biosfera Isla San Pedro 
Mart[iacute]r.
    In addition to overutilization by direct harvest, gulf grouper are 
indirectly harvested as bycatch in commercial shrimp trawls 
(Ram[iacute]rez et al. 2012) and illegal totoaba (Totoaba macdonaldi) 
fisheries (Moreno-B[aacute]ez et al. 2012). In 2012, commercial shrimp 
trawlers harvested 42,310 mt of shrimp in the GOC. Mexican shrimp 
fisheries are not required to use bycatch reduction devices (BRDs), and 
recent studies estimated the bycatch ratio (bycatch: shrimp) at 6.1:1 
(85.9 percent bycatch rate; 2003-2009) in the central GOC

[[Page 57319]]

(Meltzer 2012) and 10.2:1 (91.1 percent bycatch rate; 1992-2004) in the 
southern GOC (Madrid-Vera et al. 2007). The totoaba, currently ESA-
listed as endangered, are currently harvested via gill nets in the 
northern GOC for their swim bladders, which garner $8,500 per kg (CIRVA 
2014). Although it is unknown whether or not this totoaba fishery is 
also harvesting gulf grouper, this fishery is currently using the same 
fishing ports (i.e., San Felipe, Golfo de Santa Clara, and Puerto 
Pe[ntilde]asco) and harvest methods (i.e., gill nets) being used to 
capture gulf grouper (Moreno-B[aacute]ez et al. 2012). Estimates of 
bycatch specific to gulf grouper in the GOC shrimp trawl fishery and 
the illegal totoaba fishery are not available.
Inadequacy of Existing Regulatory Mechanisms
    In Mexico, the Comisi[oacute]n Nacional de Acuacultura y Pesca 
(CONAPESCA) has the authority to implement fishing regulations (http://www.conapescasandiego.org/contenido.cfm?cont=regulations), which are 
enforced by the Mexican Navy. Traditional fisheries regulations aimed 
at controlling catch and effort of gulf grouper in Mexican waters are 
scarce. Commercial fishing permits are only available to Mexican 
nationals and require a concession (either a cooperative or private 
business). Commercial permits are awarded per vessel for two to five 
year durations and specify species (or species group) targeted, fishing 
area, and fishing method or gears. Recreational fishing is allowed by 
national or foreign individuals through a single, non-renewable, non-
transferrable permit. In ocean waters and estuaries, a retention limit 
of ten fish is allowed per angler per day, of which only two can be 
gulf grouper. Rubber-band, spring, or pneumatic harpoons are allowed 
during recreational skin diving.
    Several marine protected areas (MPAs) have been established in 
Mexico within the gulf grouper's range. MPAs cover nearly one fifth of 
the GOC's surface area, including 101,838 hectares designated as ``no-
take'' areas (Aburto-Oropeza et al. 2011). Despite the establishment of 
multiple MPAs throughout the GOC over the past few decades, overall 
protection of fisheries resources is still inadequate for the recovery 
of overexploited stocks. The lack of management plans, effective 
regulations, and necessary resources to operationalize and enforce MPAs 
in the GOC significantly undermines their conservation benefits 
(Cudney-Bueno et al. 2009, Rife et al. 2013, Cinti et al. 2014). The 
large majority of the areas covered by GOC MPAs are still actively 
fished year-round with little or no regulations limiting harvest 
(Rodr[iacute]guez-Quiroz et al. 2010, Moreno-B[aacute]ez et al. 2012). 
The lack of adequate enforcement is a chronic and pervasive problem for 
several MPAs within the GOC. For example, one study of the Reserva de 
la Biosfera Isla San Pedro Mart[iacute]r, conducted from 2003 through 
2008, found that 39 percent of the time sport and commercial fishermen 
were fishing in the 900 hectare core no-take zone, including a large 
sport fishing derby targeting gulf grouper in 2004 (Cudney-Bueno et al. 
2009).
    With the exception of the Parque Nacional Cabo Pulmo, fish species 
diversity and biomass have not increased within designated GOC MPAs 
(Aburto-Oropeza et al. 2011). The Parque Nacional Cabo Pulmo, located 
on the southern tip of the Baja California peninsula, was established 
in 1995 to protect the large coral communities found there (Aburto-
Oropeza et al. 2011). The park includes a 2,501 hectare no-take reserve 
(35 percent of the total park area). In a ten-year study, fish species 
richness and biomass significantly increased from 1999 to 2009, and 
previous studies have found gulf grouper inhabit park waters (Aburto-
Oropeza et al. 2011). The conservation benefits of Cabo Pulmo are 
threatened by development from the tourist industry, as several large-
scale resorts have recently been proposed for this area.
    In the U.S., the California Fish and Game Commission adopted a 
regulation prohibiting the take or possession of gulf grouper in 1976 
(Title 14, Section 28.12). This regulation went into effect on March 1, 
1977, and remains in effect today.
Extinction Risk Assessment
    Gulf grouper are particularly susceptible to overfishing due to a 
combination of life history traits and behavioral characteristics 
(Sadovy de Mitcheson et al. 2012). Biological factors that likely 
increase the gulf grouper's intrinsic vulnerability to overfishing 
include large size, late onset of reproductive maturity, slow growth 
rate, and long life-span. As a protogynous hermaphrodite, the gulf 
grouper may be even more susceptible to fishing which, through 
selective removal of males, could reduce reproductive capacity. As a 
transient aggregate spawner, gulf grouper are highly susceptible to 
fishing overutilization due to the predictability of their locations in 
time and space. Once a year, adult gulf grouper aggregate for 
reproduction at a known time (full moon in May), at known locations 
(particular reefs and seamounts), at higher than normal densities. Some 
historical gulf grouper spawning aggregation sites have completely 
disappeared following heavy harvest (e.g. Punta Lobos and San Bruno 
seamounts) (S[aacute]enz-Arroyo et al. 2005a). An analysis of 2002 and 
2003 harvest data from Bah[iacute]a de Los Angeles showed that 99 
percent of the gulf grouper harvested were immature-sized fish, 
demonstrating the lack of reproductive age fish (Aburto-Oropeza et al. 
2008). Overall, the combination of high harvest rates at known spawning 
aggregation sites and the trait of protogynous hermaphroditism 
significantly impacts gulf grouper productivity. Finally, gulf grouper 
have a small geographic range, which may restrict their ability to move 
and adapt to environmental changes (Morris et al. 2000).
    Based upon the best available cumulative information from fisheries 
statistics, LFK, anecdotal reports, and grey literature, we conclude 
that gulf grouper abundance has severely declined since the mid-20th 
century due primarily to direct harvest by commercial and artisanal 
fisheries (Sala et al. 2004, S[aacute]enz-Arroyo et al. 2005a, Aburto-
Oropeza et al. 2008). The primary signs of population decline are: (1) 
Sharp reductions in harvest volumes, (2) significant decrease in 
average size and weight of harvested fish, (3) reduced spatial 
distribution and likely range contraction, and (4) extirpations or 
reductions of spawning aggregations (S[aacute]enz-Arroyo et al. 2005a, 
Aburto-Oropeza et al. 2008). In the GOC, gulf grouper were once 
abundant and represented approximately 45 percent of the artisanal 
fishery in 1960, but declined to 10 percent by the 1970s, and are now 
less than 1 percent of the fishery (S[aacute]enz-Arroyo et al. 2005a). 
The sharp decrease in harvest levels since the 1970s was not due to 
decreased fishing effort (fishing effort has generally increased) or 
new protective regulations (which are of limited benefit), but rather 
was due to a decline in gulf grouper abundance. Commercial landings of 
gulf grouper from the Pacific Ocean (U.S. vessels fishing in Mexican 
waters) peaked in the early 1950s, before the population declined to 
near commercial extinction by 1970. Based on recent fishery independent 
surveys and fisheries data, the gulf grouper has not recovered and is 
still considered a very rare occurrence in the Pacific Ocean portion of 
its range. Outside of a known population in Bah[iacute]a Magdalena 
(Octavio Aburto-Oropeza, Scripps Institution of Oceanography, pers.

[[Page 57320]]

comm., 2014), there is no published evidence of gulf grouper still 
persisting along the Pacific coast of the Baja California peninsula. 
Current gulf grouper distribution appears to be much more limited than 
their historical range (S[aacute]enz-Arroyo et al. 2005a). In the 
1930s, some irruptions of gulf groupers occurred along the San Diego 
coastline (Hubbs 1948); but there are no records of any occurring in 
this area since that time.
    In addition to direct harvest, other potential threats to gulf 
grouper abundance include bycatch in the commercial shrimp and illegal 
totoaba fisheries, habitat degradation and loss from a variety of 
sources, and climate change. However, there are no studies directly 
linking these factors to the decline in gulf grouper abundance. 
Although the cumulative impact of these threats may be significant, the 
information available does not allow for an accurate assessment of the 
relative magnitude or contribution of these threats to gulf grouper 
extinction risk.
    Due to the inadequacy of existing regulatory mechanisms, there is 
no reason to expect the primary threat to gulf grouper from fisheries 
direct harvest will diminish. Traditional fisheries regulations aimed 
at controlling gulf grouper catch and directed fishing effort in 
Mexican waters are very limited. While several MPAs have been 
established in the GOC in recent years, the lack of management plans, 
effective regulations, and necessary resources to operationalize and 
enforce these MPAs significantly undermines their conservation benefit 
(Cudney-Bueno et al. 2009, Rife et al. 2013, Cinti et al. 2014). With 
the exception of the Parque Nacional Cabo Pulmo, fish species diversity 
and biomass have not increased since the establishment of GOC MPAs 
(Aburto-Oropeza et al. 2011). The conservation benefits of Cabo Pulmo 
are currently threatened by large-scale development projects. Since 
1976, the state of California has prohibited the take or possession of 
gulf grouper. However, this restriction only applies within California 
waters, which represent a very small portion of the species' historical 
range and may no longer be part of the gulf grouper's current range. 
Gulf grouper can still be harvested and landed in Mexico by U.S. 
fishing vessels.
    The gulf grouper was once considered abundant, but is now 
considered rare (Jenkins and Evermann 1889, Croker 1937, and 
S[aacute]enz-Arroyo et al. 2005a). Direct harvest is the major reason 
for gulf grouper decline (Sala et al. 2004, S[aacute]enz-Arroyo et al. 
2005a, Aburto-Oropeza et al. 2008) and, due to the lack of protective 
regulations in Mexico (no meaningful quotas nor protective regulations 
for gulf grouper), there is no reason to expect fishing to be a 
diminishing threat. Moreover, gulf grouper are intrinsically vulnerable 
to overfishing due to life history traits, including large size, late 
onset of reproductive maturity, protogynous hermaphrodite life history, 
transient aggregate spawning, slow growth rate, long life-span, and 
restricted geographic range (Sadovy de Mitcheson et al. 2012). Sharp 
decreases in harvest levels observed since the 1970s are not due to 
decreased fishing effort (fishing effort has generally increased) or 
new protective regulations (which are of limited benefit), but rather 
are due to a decline in gulf grouper abundance. Though a series of MPAs 
have been set up in the GOC, only one, Cabo Pulmo, has an enforced no-
take marine zone, and it is the only protected marine zone in the GOC 
that has seen improved marine fish life diversity and density over the 
past decade (Aburto-Oropeza et al. 2011); therefore, the MPAs are not 
anticipated to lead to a significant increase in gulf grouper 
abundance.
Protective Efforts
    In 2005, Mexico established the [Aacute]rea de Refugio Vaquita 
Marina located in the northern GOC to protect and conserve the 
critically endangered vaquita (Phocoena sinus) by prohibiting gill net 
and trammel net use (SEMARNAT 2008). This prohibition is not directly 
designed to protect gulf grouper, but gill nets and trammel nets are 
two of the more common gulf grouper harvest methods, so the prohibition 
could have the potential to benefit gulf grouper as well. However, 
bycatch of vaquita in the illegal gill net fishery for the endangered 
totoaba has continued within this MPA after implementation. In 2015, 
the Mexican federal government increased its efforts to protect vaquita 
by expanding the [Aacute]rea de Refugio Vaquita Marina six-fold to 
approximately 8,000 square kilometers. For the next two years, gill 
nets and long lines will be prohibited within the MPA; and fishermen 
from the nearby towns of San Felipe (Baja California, Mexico) and Golfo 
de Santa Clara (Sonora, Mexico) will be financially compensated for 
changing their harvest methods. Enforcement by the Mexican Navy will be 
increased with the additional use of enforcement boats, light aircraft, 
and drones. These new conservation measures could result in decreased 
fishing pressure on gulf grouper. However, these new measures are 
temporary, and there is no long-term commitment of funds for 
enforcement or financial compensation of displaced fishermen. There are 
also large uncertainties associated with the effectiveness of the 
proposed enhanced enforcement measures given pervasive non-compliance 
with Mexican fisheries regulations and the economic incentives created 
by the extremely high valued illegal totoaba fishery.
    We did not identify any other conservation efforts to protect and 
recover gulf grouper that are either underway but not yet fully 
implemented, or are only planned. Our evaluation of the conservation 
efforts identified lead us to conclude that current conservation 
efforts cannot be considered effective measures for significantly 
reducing the current gulf grouper extinction risk.
Proposed Determination
    Based on the best available scientific and commercial information, 
as summarized here and in Dennis (2015), and consideration of efforts 
being made to protect the species, we conclude that the gulf grouper, 
Mycteroperca jordani, is currently at high risk of extinction 
throughout its range. We therefore propose to list this species as 
endangered under the ESA.

Island Grouper

    The following section describes our analysis of the status of the 
island grouper, Mycteroperca fusca.
Species Description
    The island grouper was first described under the name Serranus 
fuscus by Lowe (1836) based on specimens from Madeira, Portugal. 
Diagnostic features of the island grouper include an oblong and 
compressed body with depth less than head length, lower jaw extending 
well in front of upper jaw, dorsal fin with 11 spines and 14-16 rays, 
anal fin with 3 spines and 10-12 rays with rounded margin, and caudal-
fin rear margin truncate (juveniles) to concave (adults) (Heemstra and 
Randall 1993). Adults are brownish or dark grey, with irregular pale 
blotches and spots and a prominent maxillary streak. Under stress this 
pattern may be reversed so that the head and body are pale with 
irregular dark markings. Juveniles are mottled greenish-brown with 
prominent white spots on head and body, white streaks on median fins, 
with hyaline golden pectoral fins (Craig et al. 2011). The color 
pattern of mature females from the Canary Islands suggests sexual 
dichromatism (i.e., males and females differ in color) (Bustos 2008). A 
large proportion of sexually active females have yellow pigmentation 
(dorsal fins

[[Page 57321]]

and/or chest, ventral or uniformly throughout), while males are 
uniformly brown (Bustos 2008). This species is also known to display a 
yellow (xanthic) color phase (Wirtz 2007), and a few uniformly golden 
island grouper have been reported from Madeira (Heemstra and Randall 
1993).
    For many years island grouper were confused with another closely 
related species, Mycteroperca rubra. Based primarily on differences in 
gill raker counts, Heemstra (1991) established that the species found 
in the Atlantic Macaronesian region (from the Azores to Cape Verde) was 
M. fusca (with 20-24 lower limb gill rakers), with the distribution of 
M. rubra (with 28-31 lower limb gill rakers) being limited to the west 
coast of Africa and the Mediterranean Sea (Heemstra and Randall 1993).
    The island grouper is a slow-growing, long-lived species which can 
attain maximum sizes of at least 86 cm total length (TL) and 7.8 kg 
(Bustos 2008, Bustos et al. 2010). Longevity of island grouper is 
estimated to be between 30 and 40 years (Bustos (2008, Bustos et al. 
2009). The instantaneous rate of natural mortality estimated for island 
grouper is between 0.146 and 0.158 per year (Bustos 2008). Island 
grouper length at age was described by Bustos (2008) from commercial 
catches off Gran Canaria and Fuerteventura (Canary Islands) between 
January 2004 and December 2005. Von Bertalanffy growth model parameters 
were as follows: L[infin] = 898 mm; k = 0.062 per year; and 
t0 = -3.83 years. Only 22 percent of the island grouper 
sampled were older than ten years, and the oldest fish in this study 
was around 20 years old, 50 percent less than the maximum age estimated 
by Bustos (2008). Significant differences were found between males (n = 
35) and females (n = 153) for mean age (males 10.3 years versus females 
7.1 years), L[infin] (males 952 mm versus females 888 mm), and growth 
rate k (males 0.053 per year versus females 0.063 per year) (Bustos 
2008).
    While slow growth after the first few years is typical for 
Mycteroperca, the island grouper is particularly slow-growing when 
compared to closely related species. On average, over 28 percent of 
island grouper growth was achieved by the second year; by the fourth 
year this species attains lengths of approximately half of the maximum 
length observed. In general, growth within the genus Mycteroperca tends 
to be faster in the early stages of life, slowing down considerably in 
later stages (Bullock and Murphy 1994, Manickchand-Heileman and Phillip 
2000, Strelcheck et al. 2003). Consequently, the von Bertalanffy model 
typically does not describe the growth of Mycteroperca spp. properly 
for the first few years of life, as evidenced by relatively large 
negative t0 values.
    The island grouper is a nectobenthic (i.e., free-swimming, bottom 
oriented) macrocarnivore that preys on fish, crustaceans, and 
cephalopods (Harmelin-Vivien et al. 2001, Bustos 2008). Island grouper 
are considered mobile hunters and have been observed actively exploring 
their territories for prey (Bustos 2008).
Reproductive Biology and Spawning Behavior
    Bustos et al. (2010) studied the pattern of sexual development and 
reproductive characteristics of island grouper in the Canary Islands 
based on samples of commercially harvested fish. Island grouper are a 
protogynous hermaphroditic fish. Results of histological analyses and 
demographic structure suggest a monandric protogynous sexual pattern, 
where males develop only through sex change (Bustos 2010). The length 
at which 50 percent of the population reaches sexual maturity was 
estimated at 335 mm total length (TL), or about 4 years old. Of the 
females over 398 mm TL (5-6 years old), 95 percent were considered to 
be mature. Island grouper sexual transition occurs between 428-725 mm 
TL, with 50 percent of females transformed into males at around 678 mm 
TL (Bustos 2010). The presence of females in the larger size categories 
(up to 725 mm TL) implies that the conversion (female to male) is not 
essential in all individuals. The overall sex ratio of males to females 
(1:4.9) and the sex ratio of males to mature females (1:3.4) were both 
significantly different from 1:1 (Bustos 2010).
    In the Canary Islands, reproduction is initiated in February, when 
water temperatures are around 18[deg] C, and continues through August 
or September when temperatures peak around 24-26 [deg]C (Bustos et al. 
2010). The central period of spawning, as defined by months when 50 
percent or more of females are in vitellogenesis (i.e., yolk 
deposition), is from April to July (Bustos et al. 2010). The formation 
of spawning aggregations is a common trait among groupers (Sadovy de 
Mitcheson et al. 2008). Although there are no published studies on 
island grouper reproductive behavior, spawning aggregations have been 
reported through personal communication (J.P. Barreiros, UAC/IMAR in 
Rocha et al. 2008) from two locations in the Azores.
Population Structure, Distribution, Abundance and Habitat
    The island grouper is a subtropical species (40[deg] N-10[deg] N) 
that is endemic to volcanic archipelagos of Macaronesia: Canary Islands 
(Spain), Madeira and Azores (Portugal), and Cape Verde (Heemstra and 
Randall 1993). The Canary Islands are located between 27[deg] and 
29[deg] N latitude and 13[deg] and 18[deg] W longitude at a minimum 
distance of 100 km and maximum distance of 450 km off the coast of 
Morocco. The Canary Islands archipelago is formed by seven main 
islands, with 1,379 km of coastline, a total land area of 7,447 km\2\, 
and a human population size of approximately 2.1 million (Popescu and 
Ortega-Gras 2013). The Madeira archipelago is located from 32[deg] 37' 
to 32[deg] 52' N latitude and 16[deg] 39' to 17[deg] 15' W longitude, 
754 km from the coast of Africa and 964 km southwest of Lisbon. The 
archipelago consists of the two main inhabited islands (Madeira and 
Porto Santo), with an estimated combined human population of 268,000, 
and five uninhabited islands (Desertas and Selvagens Islands). The 
Madeira archipelago has 153 km of mostly rocky and steep coastline, and 
a total land area of 801 km\2\. The Azores archipelago is located 
between 37[deg] and 40[deg] N latitude and 24[deg] and 32[deg] W 
longitude, about 1,500 km west of Lisbon and 1,900 km southeast of 
Newfoundland. It is composed of nine islands and some small islets 
(Harmelin-Vivien et al. 2001), with 667 km of coastline, a total land 
area of 2,333 km\2\, and a human population size of approximately 
246,000. The Cape Verde archipelago is located between 14[deg] and 
17[deg] N latitude and 22[deg] and 25[deg] W longitude, due west of 
Senegal, off the west coast of Africa. It is composed of ten islands 
(of which nine are inhabited) and eight islets, with 1,020 km of 
coastline, a total land area of 4,033 km\2\, and a human population 
size of approximately 531,000. There are no confirmed reports of island 
grouper off the coast of West Africa, although ichthyofauna studies are 
lacking in this region. One specimen was caught by a spearfisherman off 
Israel's coast (Heemstra et al. 2010), but there are no data confirming 
the existence of an island grouper population in the Mediterranean.
    The island grouper is a demersal species that is found 
predominantly near rocky or sandy-rocky sea-beds (Heemstra and Randall 
1993). Studies have shown a positive correlation between island grouper 
abundance and structural complexity, algal cover (Bustos 2008), and 
upright seaweed

[[Page 57322]]

cover (Sangil et al. 2013b). The habitat requirements of larval and 
juvenile island grouper are not well-studied. All groupers pass through 
a pelagic larval phase, lasting between 20-50 days, during which they 
can actively swim (Aburto-Oropeza et al. 2008). After the larval phase, 
groupers acquire juvenile characteristics during which they settle into 
shallow, coastal nursery habitats (e.g., Sargassum beds, seagrass 
areas, mangroves, and estuaries); this nursery stage can last up to two 
years.
    The overall range distribution for island grouper is considered 
restricted, defined as less than 800,000 km\2\ (Morris et al. 2000). 
The seafloor bathymetry around the Macaronesian Islands is typically 
abrupt with a narrow contiguous shelf and a steep slope plunging to 
depths of more than 1,000 meters. As a result, viable habitat for 
demersal species such as the island grouper is considerably smaller 
than on continental shores, limiting the abundance of these populations 
(Diogo and Pereira 2013a, Popescu and Ortega-Gras 2013). Based on a 
wide range of sources, Morris et al. (2000) classified the island 
grouper as having a ``narrow depth range'' defined as occurrence at 
depths typically less than 20-30 m. Although island grouper have 
occasionally been reported at greater depths (e.g., 50 m by Heemstra 
and Randall 1993; 150 m by Bustos 2008; and 200 m by Craig et al. 
2011), based on the majority of observations, it is assumed that their 
normal distribution in the water column is at depths less than 30 m.
    Historical and current island grouper population abundance is 
unknown. Available information on island grouper distribution and 
abundance is primarily from Underwater Visual Census (UVC) studies 
conducted at various locations throughout the species' range. There is 
a considerable amount of variation in island grouper mean densities 
reported in the literature. Island grouper were reported as being very 
rare (0.03-0.10 fish/100 m\2\) in two UVC studies of benthic fish 
communities in the Azores (Harmelin-Vivien et al. 2001, Bertoncini et 
al. 2010). Compared to the Azores, a relatively higher mean density of 
island grouper (0.825 fish/100 m\2\) was reported from a single study 
in Cape Verde (Freitas 2012). However, since sampling was conducted 
within the only operationalized MPA in Cape Verde, on the uninhabited 
island of Santa Luzia (UNDP 2010), island grouper mean density from 
this study may not be representative of more heavily fished areas 
throughout the archipelago. Based on limited information, island 
grouper appear to be rare around Madeira Island, with the possible 
exception of within the Garajau Marine Reserve (Ribeiro et al. 2005, 
Ribeiro 2008). Island grouper mean densities were highly variable in 
studies conducted around the Canary Islands. The highest mean densities 
were reported around the lightly fished, remote island of El Hierro and 
within the designated marine reserves of La Graciosa (Chinijo Islands) 
and La Palma. Island grouper were generally reported as being very rare 
on the more populous and heavily fished Canary Islands of Gran Canaria 
and Tenerife.
Summary of Factors Affecting the Island Grouper
    Available information regarding current, historical, and potential 
future threats to the island grouper was thoroughly reviewed (Salz 
2015). We summarize information regarding threats below according to 
three (out of five) factors specified in section 4(a)(1) of the ESA: 
``Present or Threatened Destruction, Modification, or Curtailment of 
its Habitat or Range''; ``Overutilization for Commercial, Recreational, 
Scientific, or Educational Purposes''; and ``Inadequacy of Existing 
Regulatory Mechanisms.'' We found very little information regarding 
potential threats under the section 4(a)(1) factors ``Disease and 
Predation'' or ``Other Natural or Manmade Factors.'' These areas are 
data poor, but there are no serious or known concerns raised under 
these threat categories with respect to island grouper extinction risk; 
therefore, we do not discuss these categories further here. See Salz 
(2015) for a more detailed discussion of all ESA section 4(a)(1) threat 
categories.
Present or Threatened Destruction, Modification, or Curtailment of Its 
Habitat or Range
    Demersal fish populations around volcanic islands may be 
particularly vulnerable to habitat related threats, as they are 
typically confined to a narrow band within a few kilometers from shore 
due to the surrounding bathymetry. Various human activities throughout 
the Macaronesian region can negatively impact near-shore, rocky marine 
habitats occupied by island grouper. Increased anthropogenic pressure 
on the more densely populated Macaronesian Islands (Madeira Island, and 
Tenerife and Gran Canaria in the Canary Islands) has resulted in 
continuous modification and degradation of inshore habitats, placing 
new and unprecedented demands on coastal marine resources (Hajagos and 
Van Tassell 2001, Ribeiro 2008). Potential threats to island grouper 
habitat include ecosystem changes driven by overfishing, dynamite 
fishing, physical alteration of the coast, pollution, the effects of 
global climate change, and the introduction of invasive species.
    The island grouper is primarily found near the ocean bottom in 
areas with high structural complexity (or ``roughness'') and benthic 
cover (Bustos 2008, Monteiro et al. 2008, Sangil et al. 2013b). Canopy-
forming macroalgae are a principal engineer organism on shallow rocky 
bottoms, providing the necessary habitat complexity and benthic cover 
to support and maintain equilibrium of natural assemblages 
(Hern[aacute]ndez et al. 2008, Clemente et al. 2010, Sangil et al. 
2013b). Canopy-forming macroalgae may also ameliorate the effects of a 
range of disturbances on understory assemblages, thus enhancing the 
resistance of associated systems (Bertocci et al. 2014). The loss of 
canopy-forming macroalgae, and consequent increased environmental 
stress on associated organisms, could result in drastic reduction or 
local extinction of understory species unable to survive harsh 
environmental conditions without the protective canopy (Bertocci et al. 
2014). In the Canary Islands, the natural balance between seaweeds, 
herbivores, and predators has been disturbed due to the fishing 
depletion of predators (e.g., sparids and labrids) of the sea urchin 
(Diadema africanum), the most important herbivore of sublittoral rocky 
bottoms (Hern[aacute]ndez et al. 2008, Clemente et al. 2011). This has 
resulted in an ecosystem imbalance whereby sea urchin populations have 
increased, while cover of upright seaweeds and canopy-forming 
macroalgae have decreased (Tuya et al. 2004, Hernandez et al. 2008, 
Clemente et al. 2011, Riera et al. 2014). Seaweed beds have declined 
throughout much of the Canary Islands archipelago and are now found in 
abundance only in restricted fishing areas, remote islands, or areas 
where prevailing winds and currents limit fishing pressure (Sangil et 
al. 2013b). Steady declines in benthic cover of the canopy-forming 
brown macroalgae (Fucus spiralis and Cystoseira spp.) in the Canary 
Islands have been linked to growing sea urchin populations in 
combination with rising sea surface temperatures (Hern[aacute]ndez et 
al. 2008). Population declines and increased fragmentation of the 
endemic red alga (Gelidium canariense) have also been observed in 
Tenerife and Gran Canaria during the last 20 years (Bouza et al. 2006). 
These studies suggest that, in addition to the direct impact of fishery 
removals of island grouper, fishing can

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initiate trophic cascades that may modify and degrade island grouper 
habitats or preferred microhabitats.
    Large-scale coastal development began in the Canary Islands in the 
early 1970s to meet the needs of a growing tourist industry (Hajagos 
and Van Tassell 2001). Similarly, the Madeira Island coast has been 
extensively armored and developed in the past two decades (Ribeiro 
2008). Artificial harbors, marinas, beaches, ripraps, rubble mounds, 
and hotels were constructed on these islands, with few environmental 
precautions, resulting in massive alterations to the shoreline and 
siltation of nearshore benthic communities (Hajagos and Van Tassell 
2001). Baseline (pre-development) studies of the near-shore marine 
communities in these heavily developed areas are lacking and, 
therefore, the impacts of these habitat changes on marine fish 
populations in general, and the island grouper in particular, are 
largely unknown.
    Pollution from a variety of sources also threatens marine 
ecosystems in the Macaronesian region. In the Canary Islands, land-
based sources of pollution include organic and inorganic pollutants 
from developed areas and farms (mainly banana and tomato), brine 
releases from desalination plants, and thermal pollution from power 
plants (Riera et al. 2014). Other sources include nitrogenous waste 
from aquaculture, pollution derived from ship traffic, and extraction 
of construction materials from the seabed (Riera et al. 2014). In the 
Canary Islands, sharp declines in red alga (Gracilaria cervicornis) 
coverage over the last 10 years have been linked to coastal pollution 
from desalination plants and sewage from pipelines (Riera et al. 2014). 
On the island of Madeira, pollution from raw sewage discharges, sand 
mining, and sediment run-off severely decreases water clarity, which 
affects algae production (Ribeiro 2008). The direct impacts of 
different pollution sources on demersal fish populations in the 
Macaronesian region are not well-studied. The presence of continuous 
coastal currents around islands in this region likely facilitates the 
dispersion of pollutants (Riera et al. 2014). Thus, while localized 
impacts may be acute near highly concentrated point sources, broader 
and long lasting impacts of coastal pollution in this region have not 
been identified.
    Certain changes are likely to occur in the world's oceans due to 
long-term changes in global mean temperature and possible anthropogenic 
impacts that could pose potential future threats to island grouper 
habitats. Warmer oceanographic conditions associated with climate 
change (combined with overfishing) have likely contributed to the sea 
urchin population increase discussed above (Hern[aacute]ndez et al. 
2010). In addition, Brito et al. (2005) found 24 out of the 30 new 
records of littoral bony fishes reported between 1991 and 2005 from two 
Canary Island marine reserves (La Graciosa in Chinijo Islands and La 
Restinga in El Hierro) were species with tropical origins. The 
emergence of tropical species in subtropical latitudes has also been 
reported in Madeira and the Azores (Brito et al. 2005). However, the 
impact of progressive tropicalization of Macaronesian marine ecosystems 
on island grouper survival is widely unknown.
    The introduction of invasive species through aquaculture poses a 
potential threat to island grouper. Total production of marine finfish 
in open-net cages increased in the Canary Islands from 1,685 mt in 2001 
to 7,900 mt in 2009 (APROMAR 2012). A massive escape event occurred at 
an aquaculture operation on La Palma between December 2009 and January 
2010 resulting in the accidental release of 1.5 million fish (90 
percent European sea bass and 10 percent sea bream) into the wild 
(Toledo-Guedes et al. 2014). As an opportunistic, high trophic level, 
piscivorous species, non-native European sea bass could be competing 
with native species such as the island grouper (Toledo-Guedes et al. 
2009). Toledo-Guedes et al. (2012) found evidence of gonadal maturation 
occurring in the wild in escaped male and female European sea bass in 
the Canary Islands. The combination of suitable biotic and non-biotic 
conditions, high frequency of escape events (Toledo-Guedes et al. 
2009), and overutilization of native fish assemblages (Tuya et al. 
2006a) could facilitate establishment of self-reproducing non-native 
European sea bass populations within the island grouper's range. 
However, studies indicating that aquaculture escape events have 
resulted in a decline in island grouper abundance are lacking.
    The introduction of invasive species through ship ballast water is 
also a potential threat to the island grouper. Approximately 30,000 
commercial vessels enter Canarian harbors each year, mostly in Gran 
Canaria and Tenerife (ISTAC 2013 in Riera et al. 2014). The African 
hind (Cephalopholis taeniops) is an invasive species from Guinea (West 
Africa) that is thought to have arrived in the Canary Islands in 
ballast water (Riera et al. 2014). Stable populations of this predatory 
fish may have already established in the port cities of Las Palmas and 
Santa Cruz (Riera et al. 2014). However, as with the European sea bass, 
there are no studies indicating that the invasive African hind has 
negatively impacted native fish populations.
Overutilization for Commercial, Recreational, Scientific, or 
Educational Purposes
    Island grouper are highly susceptible to overfishing due to their 
limited range and a combination of life history characteristics 
including very slow growth, late maturation, large size, and long life 
span (Bustos 2008, Bustos et al. 2009, Saavedra 2011, Diogo and Pereira 
2013a). Saavedra (2011) used a scale developed by the Food and 
Agriculture Organization (FAO) to characterize fishing vulnerability of 
target species in the Canary Islands. Input parameters used for this 
scale included age at maturity, longevity, ratio of natural to total 
mortality, growth rate, sexual strategy, and sex ratio. Island grouper 
vulnerability was rated as either ``high'' or ``very high'' for all six 
parameters individually, and ``very high'' overall. Certain behavioral 
traits, which are common in groupers, may also add to this species' 
vulnerability to fishing. Territoriality, site specificity, and the 
formation of spawning aggregations often result in groupers being an 
easy target for fishermen (Randall and Heemstra 1991, Domeier and Colin 
1997), although these traits have not been studied or well documented 
in the island grouper. Spawning aggregations, in particular, are highly 
vulnerable to fishing due to their spatial and temporal predictability 
and to the large increase in catchability that often occurs when fish 
aggregate (Sadovy and Domeier 2005). Although information on island 
grouper spawning aggregations is lacking, there are documented examples 
of sharp population declines resulting from fisheries specifically 
targeting aggregations of other grouper species (Colin 1992, Sala et 
al. 2001, Hamilton and Matawai 2006, Sadovy de Mitcheson et al. 2012). 
The economic value of island grouper is also a factor that likely 
contributes to overutilization of this species. The island grouper is 
highly prized by commercial and artisanal fishermen for the quality of 
their flesh and typically fetch high market prices (Heemstra and 
Randall 1993, Ribeiro 2008).
    In protogynous hermaphrodites, such as the island grouper, the 
largest individuals are, in order, terminal males, individuals 
undergoing sexual transition, and the largest females next in line for 
sexual transition. Selective

[[Page 57324]]

removal of these groups at high rates can lead to decreased 
productivity of a population. Island grouper may be particularly 
vulnerable to over-fishing due to the reduction in the species' 
potential reproductive capacity caused by the decrease in the number of 
males in the population (Huntsman and Schaaf 1994, Bustos et al. 2010). 
As the relative numbers of terminal males fall, females may have 
difficulty finding a terminal male to spawn with even if some remain 
(Hawkins and Roberts 2003). In addition, sexual transition takes time 
and energy, including energy expended on social interactions and 
competition among females vying for dominance. Since removal of 
terminal males by fishing will result in more sexual transitions, 
overall population fitness may be negatively impacted.
    Historical commercial and artisanal fisheries data are not 
available to evaluate long-term trends in island grouper landings, 
directed effort, or catch rates over time. The limited landings data 
available for more recent years indicate that island grouper are 
currently a very minor component of commercial and artisanal fisheries 
throughout its range. The nearshore demersal fishery in the Canary 
Islands is artisanal, consisting primarily of small boats (Saavedra 
2011). Fishing methods used to catch demersal species include hook and 
line, fish traps, trammel nets, and gill nets (Bustos et al. 2009). 
Significant declines in populations of tunas and other pelagics since 
the 1970s have contributed to the increased pressure on coastal 
demersal species (Moreno-Herrero 2011). In addition, in the 1980s the 
Moroccan government restricted European Union vessel access to the 
Canary-Saharan Bank fishing grounds, resulting in a shift in fishing 
effort by the Canary artisanal fleet to coastal species (Pascual-
Fernandez and Diaz 1991 in Moreno-Herrero 2011). While landings volume 
of demersal species in the Canary Islands are relatively small compared 
to landings of pelagic species, these resources often have high 
economic value (i.e., price per pound) as well as cultural value. In 
2011, demersal fish species accounted for 16.7 percent of the total 
fishery landings weight but 33.2 percent of the landing value in the 
Canary Islands (Popescu and Ortega-Gras 2013). Canary Islands landings 
data prior to 2006 are only available from one port (Puerto de Mogan on 
Gran Canaria), and effort data are not available at all. Solari et al. 
(2003) reported landings of island grouper in the multi-species trap 
fishery from Puerto de Mogan for the period 1989-1999. Average monthly 
landings (for months with data available) of island grouper were 46 
fish. Detailed monthly data were not available to assess trends in 
island grouper landings over time. Island grouper accounted for about 
2.3 percent of the total catch in numbers of fish over this time 
period. Given their relatively large size and market price, it is 
likely that the proportional contribution of island grouper to the 
landings weight and value in the Gran Canaria trap fishery is 
considerably greater. Bustos et al. (2009) found very few island 
grouper greater than ten years old in commercial catches from Gran 
Canaria and Fuerteventura between January 2004 and December 2005. For a 
species with a life-span between 30-40 years, these results suggest 
that the island grouper is experiencing a high rate of fishing 
mortality in the more populated areas within the Canary Islands 
archipelago.
    Island grouper are considered an important component of the small 
artisanal fishery on El Hierro, where fish traps are banned and 
demersal species are mainly caught with hook-and-line gears 
(Falc[oacute]n et al. 2007a). Falc[oacute]n et al. (2007c) compared 
demersal species landings on El Hierro Island in the period before and 
after implementation of the La Restinga Marine Reserve. From 1990-1995 
(before implementation) a total of 700 island grouper were landed 
(116.7 fish per year). From 1997-2005 (after implementation) a total of 
1,239 island grouper were landed (137.7 fish per year). Over the entire 
period (1990-2005), island grouper were the 9th most abundant species 
landed in numbers of fish.
    In the Azores archipelago, the bottom longline and handline 
artisanal fishery for demersal species accounts for a significant 
portion of the total fishery landings, and is by far the highest valued 
fishery (Morato 2012). Annual landings by this fishery sector are 
consistently around 4,000 mt from 2000 through 2010 (Morato 2012). By 
comparison, reported landings of island grouper for the Azores 
archipelago were less than 1 mt for every year from 2001-2013 (INE 
2015). Official data from the Portugal National Institute of Statistics 
(INE) indicates a sharp and steady decline in combined ``grouper'' 
landings in the Azores from a high of 99 mt in 2003 to a low of 26 mt 
in 2013. The combined grouper category includes species of Epinephelus 
and Mycteroperca. Although island grouper landings account for a very 
minor component of combined grouper landings, this declining trend 
suggests that groupers, in general, are being overfished, which would 
likely have negative implications for the island grouper. Without 
effort data, it is not possible to say definitively that the decrease 
in landings is due to a decline in population abundance. However, total 
demersal species landings in the Azores are consistently around 4,000 
mt during the period when combined grouper landings declined 
precipitously, which suggests that directed fishing effort for demersal 
species did not decline.
    The Cape Verde artisanal fishery typically lands between 4,000 mt 
and 5,000 mt of fish annually, of which about 1,000 mt are demersal 
species (PRAO--CV 2012). Since 1992, the Cape Verde National Institute 
for Fisheries Development (INDP) has compiled data on fishing catch and 
effort for the more important artisanal fishery target species (Medina 
et al. 2007). However, as a small component of the total catch, island 
grouper are not one of the species monitored or reported in INDP 
official statistics (Albertino Martins, personal communication). A 
recent assessment of mackerel scad (Decapterus macarellus), bigeye scad 
(Selar crumenophthalmus), and black spot picarel (Spicara melanurus) 
indicates that stocks of commercially important small pelagics are 
either fully exploited or overexploited in Cape Verde (DeAlteris 2012). 
Continued overfishing of these stocks could result in added fishing 
pressure on demersal species in Cape Verde. In Madeira, demersal 
species account for less than one percent of total fisheries landings 
(Morato 2012). Reported landings of island grouper in Madeira are less 
than 1 mt per year for all years from 2000-2013 (INE 2015).
    Island grouper are also targeted in recreational and subsistence 
fisheries, and there are indications that these sectors are expanding 
rapidly in some parts of the species' range. Recreational fishing 
pressure has increased in the past few decades as a direct result of 
human population growth and a growing tourism sector (Sangil et al. 
2013b). For example, the number of recreational spearfishing licenses 
sold in S[atilde]o Miguel Island (Azores) increased from 138 in 1995 to 
717 in 2011; and the number of recreational fishing licenses sold in 
the Canary Islands more than doubled from 48,000 in 2005 to 116,000 in 
2011 (Diogo and Pereira 2013a, Castro 2014). There are also indications 
that Spain's economic crisis and growing unemployment have resulted in 
increased levels of subsistence fishing and poaching in the Canary 
Islands (Moreno-Herrero 2011). In Cape Verde, subsistence catches have 
shown an increasing trend in recent years, suggesting increased 
dependence on

[[Page 57325]]

fish as a source of food, and possibly related to declines in 
agricultural production due to climate change induced droughts 
(Trindade-Santos et al. 2013).
    Recreational and subsistence fishery landings data are lacking, as 
there are no monitoring programs for these fishery sectors throughout 
the Macaronesian Islands. Jimenez-Alvarado (2010, in Saavedra 2011) 
estimated total recreational fishery landings in the Canary Islands 
based on license sales by fishing mode, number of recreational fishing 
vessels, and limited recreational catch and effort survey data. Results 
suggest that recreational fisheries have a significant impact on fish 
populations, and on three islands (Gran Canaria, Gomera, and 
Fuerteventura) recreational landings of benthic-demersal species likely 
exceed artisanal fishery landings. Although species level recreational 
landings data are not available, this study indicates that the Canary 
Islands recreational fishery likely has an impact on island grouper 
abundance.
    Diogo and Pereira (2013a) conducted a characterization study of 
spearfishing activity in Ponta Delgada, the capital of S[atilde]o 
Miguel Island, the most populated island in the Azores archipelago. 
From August 2001 through May 2002, they recorded data from 220 
spearfishing trips (out of an estimated 281 total spearfishing trips 
taken). A total of nine island grouper were captured throughout the 
study period. By weight, island grouper accounted for less than one 
percent of the total biomass of finfish captured with spear guns in the 
survey. The mean length of island groupers captured (38 cm TL) was only 
slightly larger than the size at first maturity. Results from this 
survey, in general, suggest that abundances of species vulnerable to 
fishing (including island grouper) within the study site have been 
significantly reduced due to heavy fishing pressure (Diogo and Pereira 
2013a).
    Diogo and Pereira (2013b) also studied impacts of recreational boat 
fishing on demersal fish species off the Azores islands of Faial and 
Pico from 2004-2005. No island grouper catch were reported in a creel 
survey of 87 angler trips, and only 3 dusky grouper (E. marginatus) 
were reported. Diogo and Pereira (2013b) estimated the annual landings 
of all species by the recreational boat fishery on these two islands to 
be around 163 mt, which represents about 40 percent of the artisanal 
fishery landing weight in these areas. These results suggest that the 
impact of the recreational boat fishery on demersal fish communities in 
the Azores may be substantial. The absence of island grouper in the 
recreational fishing survey is consistent with UVC studies indicating 
the rareness of this species in the Azores (Harmelin-Vivien et al. 
2001, Bertoncini et al. 2010).
    Without basic fisheries time series data (e.g., catch, effort, 
sizes, and gears), it is difficult to quantitatively assess the impact 
of artisanal and recreational fishing on island grouper abundance. A 
few studies have demonstrated the negative impact of fishing by 
correlating relative fishing pressure with measures of island grouper 
abundance based on UVC sampling at different locations. Tuya et al. 
(2006a) found that, in the Canary Islands, island grouper mean density 
and mean biomass were significantly higher on islands with the lowest 
fishing pressure and lowest population density (El Hierro and Chinijo 
Islands) compared to other islands within the archipelago. Similar 
results were found for the dusky grouper, suggesting that human 
intervention in the Canary Islands has negatively impacted abundance of 
these large, slow growing species, with low population turnover rates.
    Tuya et al. (2006b) compared island grouper mean densities on El 
Hierro and the Chinijo Islands across sites with varying levels of 
protection from fishing: RI = no-take zone; ZA = reserve buffer zone, 
with only recreational fishing allowed for grouper species; and AV = 
outside reserve, with recreational and commercial fishing permitted, 
except fish traps, which are banned throughout these islands. A 
``reserve effect'' (i.e., higher abundance within than outside the 
reserve boundary) was not evident for island grouper within the El 
Hierro Restinga Reserve: i.e., no statistically significant differences 
were found in mean density between the no-take zone, the buffer zone, 
and the fishing area outside the reserve. A ``reserve effect'' was 
found within the Chinijo Islands La Graciosa Reserve: i.e., island 
grouper mean densities were statistically larger within the reserve 
(both RI and ZA zones) than in neighboring sites outside the reserve 
(AV zone). Bustos (2008) also found evidence for a ``reserve effect'' 
within La Graciosa, and she observed no island grouper in the two areas 
sampled outside the La Graciosa Reserve boundary.
    Sangil et al. (2013a) studied the relationship between fishing 
pressure and conservation status at sites around La Palma Island 
(Canary Islands). Fishing effort data were collected from boat-based 
and shore-based surveys conducted twice per month for one full year at 
fishing access sites around the island. Effort data included number and 
location of deployed fish traps, active fishing boats (commercial and 
recreational), shore based fishermen, and spearfishermen. The following 
biological parameters were used as indicators of conservation status: 
Percentage of seaweed cover; mean density of the sea urchin; mean 
biomass of sea urchin predators; mean biomass of combined grouper 
species (E. marginatus, M. fusca, Serranus atricauda); and mean biomass 
of the Mediterranean parrotfish (Sparisoma cretense), a highly prized 
fishing resource and indicator of fish stock status. Data were 
collected in 2009 using a UVC point-count method at 51 sites (nine 
transects per site) around the island. The correlation between fishing 
pressure and each biological parameter, including combined grouper 
biomass, was high and negative. Sampled locations with the highest 
combined grouper mean biomass corresponded with areas of lowest fishing 
pressure--i.e., inside the La Palma MPA, particularly within the no-
take portion, where all fishing activity is prohibited. The overall 
mean grouper biomass across all sites was 303.1 g/100 m\2\, compared to 
569.9 g/100 m\2\ within the limited fishing MPA area, and 2,401.5 g/100 
m\2\ within the no-take area. Grouper were virtually absent from the 
heavily fished areas just to the north of the MPA and on the eastern 
side of the island. Although this study did not provide mean biomass 
data for groupers at the species level, island grouper accounted for 
approximately one-third of the total biomass of the three grouper 
species combined (Sangil et al. 2013b).
    Ribeiro (2008) found higher density and larger mean size of island 
grouper within the protected Garajau Marine Reserve (GMR) on Madeira 
Island compared to nearby unprotected areas with similar habitat types. 
She attributed these differences to the regulations prohibiting all 
fishing in the GMR. Before it was designated a marine reserve, the GMR 
area was subjected to heavy fishing pressure from amateur fishermen 
using explosives, gill nets, and spears (Ribeiro 2008).
Inadequacy of Existing Regulatory Mechanisms
    The nearshore demersal fisheries throughout the Macaronesian 
Islands region are lightly regulated. Although these fisheries are 
primarily small-scale and artisanal, the cumulative impact on fish 
populations can be substantial, particularly for a species such as the 
island grouper, with a restricted range and high vulnerability to 
overexploitation. There are no commercial catch quotas, daily bag

[[Page 57326]]

limits, or seasonal closures in place for island grouper in any part of 
their range. The Canary Islands is the only archipelago with a minimum 
size limit for this species, and enforcement does not appear adequate 
to address non-compliance with this regulation. Gear restrictions 
(e.g., bans on fish traps, gill nets, bottom longlines, and SCUBA) are 
in place for demersal fisheries in some areas and the use of explosives 
is widely prohibited. However, the effectiveness of gear restrictions 
is substantially reduced by inadequate enforcement, as well as a shift 
in fishing effort to other (legal) methods of capturing demersal 
species. There is some indication that banning fish traps has had a 
positive impact on island grouper abundance in the Canary Islands, 
although this ban only applies to two sparsely populated regions within 
the archipelago. Overall, it appears that current fishing regulations 
are inadequate for addressing the direct threat to island grouper from 
fisheries overutilization. Current regulations are also likely 
inadequate to control overfishing of the main sea urchin predators, 
which, based on recent studies from the Canary Islands, has resulted in 
a trophic cascade that has modified and degraded island grouper 
habitat.
    In recent decades, no-take MPAs have received increased attention 
as a conservation tool aimed at protecting vulnerable fish populations 
(Halpern and Warner 2002). For some grouper species, increased fish 
density and size within no-take reserves may increase reproductive 
potential by promoting the occurrence of spawning aggregations 
(Sanchez-Lizaso et al. 2000). The ``reserve effect'' on island grouper 
abundance (i.e., higher abundance within than outside the reserve 
boundary) was reported for one reserve on Madeira Island and two 
reserves in the Canary Islands archipelago. However, overall, the 
system of MPAs throughout the Macaronesian Islands is likely inadequate 
to protect island grouper from the threat of fishing overutilization. 
No-take zones account for only a small fraction of the total area 
covered by MPAs within the island grouper's range, as most areas still 
allow some types of fishing. In the Azores, Madeira, and Canary Islands 
archipelagos, there are only five no-take marine reserves, which occupy 
a total area of 28 km\2\ (Fenberg et al. 2012). Given their small size 
and physical isolation from one another, no-take zones may lack the 
connectivity to allow the flow of larval and juvenile fish across 
islands and archipelagos within the region (Mart[iacute]n-Garc[iacute]a 
et al. 2015). There are also no MPAs or time-area closures designed 
specifically to protect island grouper during spawning periods, and 
little is known about the timing, location, or frequency of spawning 
aggregations for this species.
Extinction Risk Assessment
    In determining an appropriate foreseeable future timeframe for the 
island grouper extinction risk assessment, we considered both the life 
history of the species and whether we could project the impact of 
threats or demographic risk factors through time. We chose 40 years as 
the foreseeable future timeframe for island grouper. Threats to island 
grouper can potentially have long-lasting impacts, given the species' 
very slow growth rate, late maturation, and long maximum life span. 
However, considering the limited information available to predict the 
impacts from threats in the future, we felt 40 years was the most 
appropriate foreseeable future timeframe for island grouper.
    Data from UVC sampling and fisheries landings indicate that the 
island grouper is rare throughout much of its limited range and very 
rare in some areas subjected to heavy fishing pressure. Of the 85 
grouper species assessed by Morris et al. (2000), the island grouper 
was one out of only four species characterized as having both a 
``restricted'' overall range and a ``narrow'' depth range. Although 
there are no population abundance estimates available for island 
grouper, low and decreased density combined with a highly restricted 
range indicate that small population size is likely a risk factor for 
this species, which could be disproportionally affected by coastal 
development or a stochastic catastrophic event. Demographic viability 
factors related to growth rate and productivity are also likely to 
contribute to the extinction risk based on the following island grouper 
life history characteristics: Slow growth, late maturation, low 
population turnover rate, large size, and long life span (Bustos 2008). 
While slow growth after the first few years is typical for species of 
Mycteroperca, the island grouper is one of the slowest growing species 
within this genus (Bustos et al. 2009).
    Although information on spatial structure, connectivity, and 
dispersal characteristics specific to island grouper is sparse, it is 
somewhat likely that these factors represent a demographic viability 
risk to this species. Island grouper are rare in many areas studied, 
and the few documented areas with relatively higher abundance are small 
and patchily distributed throughout the species' range. Typical of 
archipelago ecosystems, the Macaronesian Islands are highly fragmented, 
as geographic distances, bathymetry, and other physical factors result 
in various degrees of isolation between islands and local populations 
of demersal fish species (Medina et al. 2007). Given their geographic 
distribution and narrow depth ranges, it is likely that island grouper 
are inherently susceptible to fragmentation, and this risk factor could 
be exacerbated by further population declines. Because there is 
insufficient information on genetic diversity, this demographic 
viability criterion presents an unknown likelihood of contributing to 
the island grouper's extinction risk.
    The island grouper's intrinsic vulnerability to fishing is very 
high (Saavedra 2011, Diogo and Pereira 2013a). Demographic viability 
risk factors related to the island grouper's growth rate, productivity, 
spatial structure, and range size all contribute to this species' 
vulnerability to fishing overexploitation (Bustos 2008, Bustos et al. 
2009, Saavedra 2011, Diogo and Pereira 2013a). As a protogynous 
hermaphrodite, the island grouper may be even more susceptible to 
fishing, which, through selective removal of males, could reduce 
reproductive capacity (Huntsman and Schaaf 1994, Bustos et al. 2010). 
Certain behavioral traits (i.e., territoriality, site specificity, and 
spawning aggregations), which are common among groupers, often result 
in grouper species being an easy target for fishermen (Randall and 
Heemstra 1991, Domeier and Colin 1997). Although not well-studied in 
the island grouper, these traits may add to the fishing vulnerability 
of this species. The economic value of the island grouper is also a 
factor that likely contributes to overutilization of this species. 
Groupers are highly prized by commercial and artisanal fishermen for 
the quality of their flesh, and most species (including island grouper) 
fetch high market prices (Heemstra and Randall 1993, Ribeiro 2008).
    Historical fisheries data are not available to evaluate long-term 
trends in island grouper landings, directed effort, or catch rates over 
time. The limited commercial and artisanal catch data available 
indicate that, in recent years, island grouper landings have been 
relatively small, and this species is currently a very minor component 
of commercial and artisanal fisheries throughout its range. The small 
contribution to recent fisheries landings is consistent with abundance 
information suggesting the island grouper is generally a rare species.

[[Page 57327]]

Although fishing intensity is highly variable between islands, there 
are indications that artisanal fishing pressure for demersal species, 
in general, is relatively high in many areas throughout the island 
groupers' range. The depleted status of commercially important stocks 
of tunas and small pelagics in the Macaronesian region has also likely 
contributed to the increased fishing pressure on coastal demersal 
species in recent years (Moreno-Herrero 2011, DeAlteris 2012).
    Several studies have demonstrated a strong negative correlation 
between island grouper abundance and level of fishing pressure (Tuya et 
al. 2006a, Bustos 2008, Ribeiro 2008, Sangil et al. 2013a, Sangil et 
al. 2013b). These results suggest that fisheries overexploitation has 
negatively impacted island grouper abundance, and some heavily fished 
areas have likely experienced a sharp decline. This is particularly 
concerning for a rare species with a limited range and high intrinsic 
vulnerability to the effects of overfishing due to certain life history 
and behavioral traits. The lack of baseline abundance information and a 
time series of fishery dependent data, combined with limitations of the 
available studies, make it difficult to quantitatively assess the 
impact of this threat on island grouper abundance or species' survival. 
However, based on the cumulative information available, we conclude 
that there is a reasonable likelihood that artisanal fishing 
overutilization contributes to the island grouper's risk of extinction 
in a significant way. There are also indications that rapidly expanding 
recreational fisheries contribute significantly to the overutilization 
of island grouper in some parts of the species' range.
    Current fishing regulations designed to limit catch and effort are 
inadequate for addressing the direct threat to island grouper from 
fishing overutilization. In general, there are few restrictions placed 
on demersal fisheries throughout the island grouper's range. In areas 
where regulations (e.g., size limits and gear restrictions) do exist, 
their effectiveness is likely reduced by lack of enforcement and 
relatively high levels of non-compliance. A well-designed system of no-
take MPAs may be better suited than traditional fishing regulations for 
addressing the threat of fishing to highly vulnerable, nearshore 
demersal species. The ``reserve effect'' on island grouper abundance 
(i.e., higher abundance within than outside the reserve boundary) was 
reported for one reserve on Madeira Island and two reserves in the 
Canary Islands archipelago. However, no-take zones account for only a 
small fraction of the total area covered by MPAs within the island 
grouper's range, as most MPAs still allow some types of fishing. Given 
their small size, physical isolation from one another, and insufficient 
enforcement, the currently established marine reserves are likely 
inadequate to protect island grouper from the current and future threat 
of fishing overutilization. Overall, we conclude that there is a 
reasonable likelihood that the lack of adequate regulatory mechanisms 
and enforcement represent threats to the island grouper that contribute 
significantly to this species' extinction risk.
    Due to the species' preferred depth range and the surrounding 
volcanic island bathymetry, island grouper habitat is typically 
confined to a narrow band within a few kilometers from shore. Close 
proximity to the shore increases the risk of habitat modification from 
human activities within the coastal zone, particularly on the more 
densely populated Macaronesian Islands. Potential threats to island 
grouper habitat include: Declines in benthic cover (i.e., seaweeds and 
macroalgae) due to overfishing of key sea urchin predators; physical 
alteration and armoring of the coast; destructive fishing practices; 
pollution; and the effects of global climate change (see section 
``Present or Threatened Destruction, Modification, or Curtailment of 
Habitat or Range'' for more details). While these ecosystem 
disturbances are well documented, studies linking habitat related 
threats to declines in island grouper abundance are lacking. Although 
the cumulative impact of anthropogenic threats has likely modified some 
portion of the island grouper's habitat, there is not enough scientific 
information available to support a conclusion that habitat associated 
changes contribute to the extinction risk of this species in a 
significant way. The introduction of invasive species from aquaculture 
escape events and ship ballast water also poses a potential threat to 
island grouper through increased competition for limited resources 
(e.g., food, shelter) and the possible spread of diseases and 
parasites. However, as with habitat related threats, there is not 
enough scientific information available to support a conclusion that 
threats related to invasive species contribute to the island grouper's 
extinction risk in a significant way.
    In summary, the island grouper exhibits demographic risk factors 
related to abundance, growth rate and productivity, and spatial 
structure and connectivity. In addition, there is a reasonable 
likelihood that the operative threats of fishing overutilization and 
the lack of adequate regulatory mechanisms contribute significantly to 
the island grouper's risk of extinction.
Protective Efforts
    We evaluated conservation efforts to protect and recover island 
grouper that are either underway but not yet fully implemented, or are 
only planned. As part of the European Union (EU), the Azores, Madeira, 
and Canary Islands archipelagos are influenced by EU conservation 
initiatives and directives. In 2008, the EU adopted the Marine Strategy 
Framework Directive (MSFD) in order to achieve Good Environmental 
Status (GES) through ecosystem-based management in EU waters by 2020. 
To comply with the MSFD, member states must ensure that their 
biological and physical marine features adhere to the specific 
qualitative descriptors of GES for the maintenance of biological 
diversity, habitat quality, and sustainable harvest levels of fish and 
shellfish stocks (Fenberg et al. 2012). The establishment of a coherent 
network of MPAs is the only mandated measure of the MSFD. The emphasis 
on MPAs and biodiversity in the MSFD reinforces previously established 
commitments in the European Biodiversity Strategy and obligations under 
the international Convention on Biological Diversity (Bellas 2014). The 
adoption of the EU's MSFD policy demonstrates a general willingness to 
achieve long-term protection of Europe's marine ecosystems, but whether 
the political will is strong enough in the Macaronesian Islands to 
achieve its objectives remains to be seen (Santos et al. 2014).
    The Portuguese government approved two MSFD strategies in 2012, one 
for the continental EEZ and one for the extended continental shelf; but 
no MSFD strategy has yet been approved by the autonomous governments of 
the Azores and Madeira archipelagos (Santos et al. 2014). In Spain, the 
MSFD has resulted in passage of the 2010 Law on the Protection of the 
Marine Environment (LPME). The LPME provides a general legal framework 
for the conservation and sustainable use of marine resources, as well 
as specific language regarding the creation and management of a Spanish 
network of MPAs, including some within the Canary Islands (Bellas 
2014). Four proposed Canary Islands MPAs are currently waiting to be 
approved by the Spanish government: One on the north coast of La 
Gomera, two in Tenerife, and one on the east coast of Gran Canaria

[[Page 57328]]

(Riera et al. 2014). However, previous attempts to establish new MPAs 
in the Canary Islands have often been stalled or abandoned due to 
stakeholder opposition, political infeasibility, and lack of funding 
(Chuenpagdee et al. 2013). For example, the regional island government 
of Tenerife has been promoting the creation of MPAs on the island since 
2004. Two proposed MPAs were finally approved in 2010--six years after 
initial planning started--but to date neither one has been implemented.
    A joint United Nations Development Program (UNDP) and Global 
Environment Facility (GEF) project titled ``Consolidation of Cape 
Verde's Protected Areas System'' was initiated in 2010 in an effort to 
strengthen and expand Cape Verde's national system of terrestrial and 
marine protected areas (UNDP 2013). Project objectives include: (1) 
Consolidation, expansion, and operationalization of existing MPAs on 
the islands of Sal and Boavista for the protection of fisheries 
resources, (2) building the national capacity for MPA management 
through new management sectors and authorities, and (3) promotion of 
participatory approaches in the management and conservation of the 
endemic biodiversity of Cape Verde. The project is expected to add 
41,214 ha of terrestrial and marine protected areas (i.e., a 38 percent 
expansion over the existing baseline).
    Other regional, local and grassroots efforts are underway to 
conserve and protect marine resources in the Macaronesian Islands. 
Local nongovernmental organizations (NGOs) and regional governments in 
the Canary Islands are promoting the creation of Micro Areas 
Ecotur[iacute]sticas Litorales (MAELs). Due to their small scale, MAELs 
are less demanding on public funding, typically less contentious, and 
follow a different legal model compared to larger scale MPAs (Riera et 
al. 2014). A well-designed and enforced network of MAELs could provide 
additional conservation benefit to demersal fish populations in the 
Canary Islands. The Canarias por una Costa Viva program is a 
partnership among NGOs, universities, and local and regional 
governments. Costa Viva program objectives include studying the impacts 
of human population pressures on the coastal environment, increasing 
marine environmental education and awareness, promoting and 
facilitating stakeholder involvement in marine resource management, and 
collaborating with government agencies in the sustainable use of Canary 
Islands marine resources. The Azores University SMARTPARKS program 
(Planning and Management System for Small Islands Protected Areas) is 
aimed at facilitating the development of sustainable protected areas in 
the Azores through active involvement of stakeholders, promotion of 
economic and cultural activities compatible with nature conservation, 
and innovative planning and management of protected areas at the island 
scale (Fonseca et al. 2014).
    In summary, there are several conservation initiatives that are 
either underway but not yet fully implemented or are still in the 
planning phase that could potentially provide conservation benefits to 
the marine ecosystems within the island grouper range. However, there 
are still major uncertainties regarding whether or not these 
initiatives will be fully implemented, operationalized, and adequately 
enforced. There are also uncertainties associated with the 
effectiveness of these efforts in reducing the island grouper 
extinction risk. Large-scale programs, such as the EU's MSFD, often 
have broad, general objectives for improving marine stewardship which 
may or may not include specific measures needed for protecting a 
particular species at risk. Regional, local and grassroots efforts may 
face fewer legal, political, and social hurdles in terms of 
implementation as compared to larger scale national programs. However, 
smaller scale programs, such as MAELs, may be limited in their 
effectiveness for species protection due to their small geographic size 
and inadequate resources for long-term management and enforcement of 
conservation measures. We conclude that given large uncertainties 
associated with implementation, enforcement, and effectiveness, the 
conservation efforts identified cannot be considered reasonably likely 
to significantly reduce the current island grouper extinction risk.
Proposed Determination
    Based on the best available scientific and commercial information, 
as summarized here and in Salz (2015), and consideration of protective 
efforts being made to protect the species, we find that the island 
grouper (Mycteroperca fusca) is at a moderate risk of extinction. The 
nature of the threats and demographic risks identified, taking into 
account the uncertainty associated with the threats and risks, does not 
demonstrate the species is presently in danger of extinction; and 
therefore, it does not meet the definition of an endangered species. 
However, the current threats to island grouper from fishing 
overutilization and inadequate regulatory mechanisms are likely to 
continue in the future, further exacerbating the demographic risk 
factors associated with abundance, growth rate and productivity, and 
spatial structure and connectivity. We conclude that both the species' 
current risk of extinction and the best available information on the 
extent of, and trends in, the major threats affecting this species make 
it likely this species will become an endangered species within the 
foreseeable future (defined as 40 years) throughout its range. We 
therefore propose to list it as threatened under the ESA.

Effects of Listing

    Conservation measures provided for species listed as endangered or 
threatened under the ESA include recovery actions (16 U.S.C. 1533(f)); 
concurrent designation of critical habitat, if prudent and determinable 
(16 U.S.C. 1533(a)(3)(A)); Federal agency requirements to consult with 
NMFS under section 7 of the ESA to ensure their actions do not 
jeopardize the species or result in adverse modification or destruction 
of critical habitat should it be designated (16 U.S.C. 1536); and 
prohibitions on taking (16 U.S.C. 1538). Recognition of the species' 
plight through listing promotes conservation actions by Federal and 
state agencies, foreign entities, private groups, and individuals. The 
main effects of this rule if finalized as proposed for gulf grouper are 
prohibitions on take, including export, import, and use in foreign 
commerce.

Identifying Section 7 Conference and Consultation Requirements

    Section 7(a)(2) (16 U.S.C. 1536(a)(2)) of the ESA and NMFS/USFWS 
regulations require Federal agencies to consult with us to ensure that 
activities they authorize, fund, or carry out are not likely to 
jeopardize the continued existence of listed species or destroy or 
adversely modify critical habitat. Section 7(a)(4) (16 U.S.C. 
1536(a)(4)) of the ESA and NMFS/USFWS regulations also require Federal 
agencies to confer with us on actions likely to jeopardize the 
continued existence of species proposed for listing, or that result in 
the destruction or adverse modification of proposed critical habitat of 
those species. It is unlikely that listing the gulf grouper under the 
ESA will increase the number of section 7 consultations, because at 
present this species is only known to occur outside of the United 
States and is unlikely to be affected by Federal actions. Although

[[Page 57329]]

the gulf grouper's historical range includes parts of Southern 
California, there are no recent records indicating that this species 
still exists in U.S. waters.

Critical Habitat

    Critical habitat is defined in section 3 of the ESA (16 U.S.C. 
1532(5)) as: (1) 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. Section 4(a)(3)(A) of the ESA (16 
U.S.C. 1533(a)(3)(A)) requires that, to the extent prudent and 
determinable, critical habitat be designated concurrently with the 
listing of a species. However, critical habitat shall not be designated 
in foreign countries or other areas outside U.S. jurisdiction (50 CFR 
424.12(h)). We can designate critical habitat in areas in the United 
States currently unoccupied by the species, if the area(s) are 
determined by the Secretary to be essential for the conservation of the 
species. Regulations at 50 CFR 424.12(e) specify that we shall 
designate as critical habitat areas outside the geographical range 
presently occupied by the species only when the designation limited to 
its present range would be inadequate to ensure the conservation of the 
species.
    The best available scientific and commercial information does not 
indicate that U.S. waters provide any specific essential biological or 
physical function for the gulf grouper. U.S. waters account for a very 
small portion on the northern limit of the gulf grouper's historical 
range, and may no longer be part of the species' current range. Based 
on the best available information, we have not identified unoccupied 
areas in U.S. waters that are currently essential to the conservation 
of gulf grouper. Therefore, based on the available information, we do 
not intend to designate critical habitat for gulf grouper.
    The island grouper occurs entirely outside of the United States. 
Therefore, we cannot designate critical habitat for island grouper.

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

    On July 1, 1994, NMFS and FWS published a policy (59 FR 34272) that 
requires us to identify, to the maximum extent practicable at the time 
a species is listed, those activities that would or would not 
constitute a violation of section 9 of the ESA. Because we are 
proposing to list the gulf grouper as endangered, all of the 
prohibitions of section 9(a)(1) of the ESA will apply to this species. 
These include prohibitions against the import, export, use in foreign 
commerce, or ``take'' of the species. These prohibitions apply to all 
persons subject to the jurisdiction of the United States, including in 
the United States, its territorial sea, or on the high seas. Take is 
defined as ``to harass, harm, pursue, hunt, shoot, wound, kill, trap, 
capture, or collect, or to attempt to engage in any such conduct.'' The 
intent of this policy is to increase public awareness of the effects of 
this listing on proposed and ongoing activities within the species' 
range. Activities that we believe could result in a violation of 
section 9 prohibitions for this species include, but are not limited 
to, the following:
    (1) Possessing, delivering, transporting, or shipping any 
individual or part (dead or alive) taken in violation of section 
9(a)(1);
    (2) Delivering, receiving, carrying, transporting, or shipping in 
interstate or foreign commerce any individual or part, in the course of 
a commercial activity;
    (3) Selling or offering for sale in interstate commerce any part, 
except antique articles at least 100 years old;
    (4) Importing or exporting any individual or part; and
    (5) Harming captive animals by, among other things, injuring or 
killing a captive animal, through experimental or potentially injurious 
care or conducting research or sexual breeding activities on captive 
animals, outside the bounds of normal animal husbandry practices. 
Experimental or potentially injurious care or procedures and research 
or sexual breeding activities of gulf grouper may, depending on the 
circumstances, be authorized under an ESA 10(a)(1)(A) permit for 
scientific research or the enhancement of the propagation or survival 
of the species.

Identification of Those Activities That Would Not Constitute a 
Violation of Section 9 of the ESA

    We will identify, to the extent known at the time of the final 
rule, specific activities involving gulf grouper that will not be 
considered likely to result in a violation of section 9 of the ESA. 
Although not binding, we are considering the following actions, 
depending on the circumstances, as not being prohibited by ESA section 
9:
    (1) Take authorized by, and carried out in accordance with the 
terms and conditions of, an ESA section 10(a)(1)(A) permit issued by 
NMFS for purposes of scientific research or the enhancement of the 
propagation or survival of the species; and
    (2) Continued possession of parts that were in possession at the 
time of listing. Such parts may be non-commercially exported or 
imported; however the importer or exporter must be able to provide 
evidence to show that the parts meet the criteria of ESA section 
9(b)(1) (i.e., held in a controlled environment at the time of listing, 
in a non-commercial activity).
    Section 11(f) of the ESA gives NMFS authority to promulgate 
regulations that may be appropriate to enforce the ESA. NMFS may 
promulgate future regulations to regulate trade or holding of gulf 
grouper, if necessary. NMFS will provide the public with the 
opportunity to comment on future proposed regulations.

Protective Regulations Under Section 4(d) of the ESA

    We are proposing to list the island grouper as a threatened 
species. In the case of threatened species, ESA section 4(d) leaves it 
to the Secretary's discretion whether, and to what extent, to extend 
the section 9(a) ``take'' prohibitions to the species, and authorizes 
us to issue regulations necessary and advisable for the conservation of 
the species. Thus, we have flexibility under section 4(d) to tailor 
protective regulations, taking into account the effectiveness of 
available conservation measures. The 4(d) protective regulations may 
prohibit, with respect to threatened species, some or all of the acts 
which section 9(a) of the ESA prohibits with respect to endangered 
species. These 9(a) prohibitions apply to all individuals, 
organizations, and agencies subject to U.S. jurisdiction. Since the 
island grouper occurs entirely outside of the United States, and is not 
commercially traded with the United States, extending the section 9(a) 
``take'' prohibitions to this species will not result in added 
conservation benefits or species protection. Therefore, we do not 
intend to issue section 4(d) regulations for the island grouper.

[[Page 57330]]

Public Comments Solicited

    To ensure that any final action resulting from this proposed rule 
to list two species will be as accurate and effective as possible, we 
are soliciting comments and information from the public, other 
concerned governmental agencies, the scientific community, industry, 
and any other interested parties on information in the status review 
and proposed rule. Comments are encouraged on these proposals (See 
DATES and ADDRESSES). We must base our final determination on the best 
available scientific and commercial information when making listing 
determinations. We cannot, for example, consider the economic effects 
of a listing determination. Final promulgation of any regulation(s) on 
these species' listing proposals will take into consideration the 
comments and any additional information we receive, and such 
communications may lead to a final regulation that differs from this 
proposal or result in a withdrawal of this listing proposal. We 
particularly seek:
    (1) Information concerning the threats to either of the two species 
proposed for listing;
    (2) Taxonomic information on either of these species;
    (3) Biological information (life history, genetics, population 
connectivity, etc.) on either of these species;
    (4) Efforts being made to protect either of these species 
throughout their current ranges;
    (5) Information on the commercial trade of either of these species; 
and
    (6) Historical and current distribution and abundance and trends 
for either of these species.
    We request that all information be accompanied by: (1) Supporting 
documentation, such as maps, bibliographic references, or reprints of 
pertinent publications; and (2) the submitter's name, address, and any 
association, institution, or business that the person represents.

Role of Peer Review

    In December 2004, the Office of Management and Budget (OMB) issued 
a Final Information Quality Bulletin for Peer Review establishing a 
minimum peer review standard. Similarly, a joint NMFS/FWS policy (59 FR 
34270; July 1, 1994) requires us to solicit independent expert review 
from qualified specialists, concurrent with the public comment period. 
The intent of the peer review policy is to ensure that listings are 
based on the best scientific and commercial data available. We 
solicited and received peer review comments on each of the status 
review reports, including from: three marine scientists with expertise 
on the gulf grouper, and three marine scientists with expertise on the 
island grouper. Peer reviewer comments for each species are 
incorporated into the draft status review reports and this 12-month 
finding.

References

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

Classification

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 (NEPA) (See NOAA Administrative Order 216-6).

Executive Order 12866, Regulatory Flexibility Act, and Paperwork 
Reduction Act

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

Executive Order 13132, Federalism

    In accordance with E.O. 13132, we determined that this proposed 
rule does not have significant Federalism effects and that a Federalism 
assessment is not required. In keeping with the intent of the 
Administration and Congress to provide continuing and meaningful 
dialogue on issues of mutual state and Federal interest, this proposed 
rule will be given to the relevant governmental agencies in the 
countries in which these two species occur, and they will be invited to 
comment. We will confer with the U.S. Department of State to ensure 
appropriate notice is given to foreign nations within the range of both 
species. As the process continues, we intend to continue engaging in 
informal and formal contacts through the U.S. State Department, giving 
careful consideration to all written and oral comments received.

List of Subjects

50 CFR Part 223

    Endangered and threatened species, Exports, Transportation.

50 CFR Part 224

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

    Dated: September 14, 2015.
Samuel D. Rauch III,
Deputy Assistant Administrator for Regulatory Programs, National Marine 
Fisheries Service.

    For the reasons set out in the preamble, 50 CFR parts 223 and 224 
are proposed to be amended as follows:

PART 223--THREATENED MARINE AND ANADROMOUS SPECIES

    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).

    2. In Sec.  223.102, in paragraph (e), the table is amended by 
adding an entry for ``Grouper, island'' under Fishes in alphabetical 
order by common name to read as follows:


Sec.  223.102  Enumeration of threatened marine and anadromous species.

* * * * *
    (e) * * *

[[Page 57331]]



--------------------------------------------------------------------------------------------------------------------------------------------------------
                                       Species \1\
-----------------------------------------------------------------------------------------  Citation(s) for listing
                                                                  Description of listed       determination(s)       Critical habitat      ESA rules
             Common name                    Scientific name               entity
--------------------------------------------------------------------------------------------------------------------------------------------------------
 
                                                                      * * * * * * *
--------------------------------------------------------------------------------------------------------------------------------------------------------
                                                                         Fishes
--------------------------------------------------------------------------------------------------------------------------------------------------------
 
                                                                       * * * * * *
Grouper, island......................  Mycteroperca fusca......  Entire species.........  [Insert Federal Register                 NA                 NA
                                                                                           citation], 9/23/2015.
 
                                                                      * * * * * *
--------------------------------------------------------------------------------------------------------------------------------------------------------
\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).

* * * * *

PART 224--ENDANGERED MARINE AND ANADROMOUS SPECIES

    3. The authority citation for part 224 continues to read as 
follows:

    Authority:  16 U.S.C. 1531-1543 and 16 U.S.C. 1361 et seq.

    4. In Sec.  224.101, in paragraph (h), the table is amended by 
adding an entry for ``Grouper, gulf'' under Fishes in alphabetical 
order by common name to read as follows:


Sec.  224.101  Enumeration of endangered marine and anadromous species.

* * * * *
    (h) * * *

--------------------------------------------------------------------------------------------------------------------------------------------------------
                                       Species \1\
-----------------------------------------------------------------------------------------  Citation(s) for listing
                                                                  Description of listed       determination(s)       Critical habitat      ESA rules
             Common name                    Scientific name               entity
--------------------------------------------------------------------------------------------------------------------------------------------------------
 
                                                                      * * * * * * *
--------------------------------------------------------------------------------------------------------------------------------------------------------
                                                                         Fishes
--------------------------------------------------------------------------------------------------------------------------------------------------------
 
                                                                      * * * * * * *
Grouper, gulf........................  Mycteroperca jordani....  Entire species.........  [Insert Federal Register                 NA                 NA
                                                                                           citation], 9/23/2015.
 
                                                                      * * * * * *
--------------------------------------------------------------------------------------------------------------------------------------------------------
\1\ Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement, see 61 FR 4722, February 7, 1996), and
  evolutionarily significant units (ESUs) (for a policy statement, see 56 FR 58612, November 20, 1991).

* * * * *
[FR Doc. 2015-23502 Filed 9-22-15; 8:45 am]
 BILLING CODE 3510-22-P



                                                57314             Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules

                                                  Issued in Kansas City, Missouri, on                   ADDRESSES:   You may submit comments                  February 21, 2014; and 79 FR 10104,
                                                September 14, 2015.                                     on this document, identified by the code              February 24, 2014). This document
                                                Mel Johnson,                                            NOAA–NMFS–2015–0071, by either of                     addresses the 12-month findings for two
                                                Acting Manager, Small Airplane Directorate,             the following methods:                                of these species: Gulf grouper
                                                Aircraft Certification Service.                            • Electronic Submission: Submit all                (Mycteroperca jordani) and island
                                                [FR Doc. 2015–24161 Filed 9–22–15; 8:45 am]             electronic public comments via the                    grouper (Mycteroperca fusca). The
                                                BILLING CODE 4910–13–P                                  Federal eRulemaking Portal. Go to                     status of the findings and relevant
                                                                                                        www.regulations.gov/                                  Federal Register notices for the other 21
                                                                                                        #!docketDetail;D=NOAA-NMFS-2015-                      species and 3 subpopulations can be
                                                                                                        0071. Click the ‘‘Comment Now’’ icon,                 found on our Web site at http://
                                                DEPARTMENT OF COMMERCE                                                                                        www.nmfs.noaa.gov/pr/species/
                                                                                                        complete the required fields. Enter or
                                                National Oceanic and Atmospheric                        attach your comments.                                 petition81.htm.
                                                Administration                                             • Mail: Submit written comments to,                   We are responsible for determining
                                                                                                        Ron Salz, NMFS Office of Protected                    whether species are threatened or
                                                                                                        Resources (F/PR3), 1315 East West                     endangered under the ESA (16 U.S.C.
                                                50 CFR Parts 223 and 224
                                                                                                        Highway, Silver Spring, MD 20910,                     1531 et seq.). To make this
                                                [Docket No. 150527481–5834–01]                          USA.                                                  determination, we consider first
                                                                                                           Instructions: Comments sent by any                 whether a group of organisms
                                                RIN 0648–XD971                                          other method, to any other address or                 constitutes a ‘‘species’’ under the ESA,
                                                                                                        individual, or received after the end of              then whether the status of the species
                                                Endangered and Threatened Wildlife                      the comment period, may not be                        qualifies it for listing as either
                                                and Plants: Proposed Threatened                         considered. All comments received are                 threatened or endangered. Section 3 of
                                                Status for Island Grouper                               a part of the public record and will                  the ESA defines a ‘‘species’’ to include
                                                (Mycteroperca fusca) and Endangered                     generally be posted for public viewing                ‘‘any subspecies of fish or wildlife or
                                                Status for Gulf Grouper (Mycteroperca                   on http://www.regulations.gov without                 plants, and any distinct population
                                                jordani) Under the Endangered                           change. All personal identifying                      segment of any species of vertebrate fish
                                                Species Act (ESA)                                       information (e.g., name, address, etc.),              or wildlife which interbreeds when
                                                AGENCY:  National Marine Fisheries                      confidential business information, or                 mature.’’ On February 7, 1996, NMFS
                                                Service (NMFS), National Oceanic and                    otherwise sensitive information                       and the U.S. Fish and Wildlife Service
                                                Atmospheric Administration (NOAA),                      submitted voluntarily by the sender will              (USFWS; together, the Services) adopted
                                                Commerce.                                               be publicly accessible. We will accept                a policy describing what constitutes a
                                                                                                        anonymous comments (enter ‘‘N/A’’ in                  distinct population segment (DPS) of a
                                                ACTION: Proposed rule; 12-month                                                                               taxonomic species (the DPS Policy; 61
                                                findings; request for comments.                         the required fields if you wish to remain
                                                                                                        anonymous). Attachments to electronic                 FR 4722). The DPS Policy identified two
                                                SUMMARY:   We, NMFS, announce 12-                       comments will be accepted in Microsoft                elements that must be considered when
                                                month findings and listing                              Word, Excel, or Adobe PDF file formats                identifying a DPS: (1) The discreteness
                                                determinations on a petition to list the                only.                                                 of the population segment in relation to
                                                gulf grouper (Mycteroperca jordani) and                    You can obtain the petition, status                the remainder of the species (or
                                                                                                        review reports, proposed rule, and list               subspecies) to which it belongs; and (2)
                                                the island grouper (Mycteroperca fusca)
                                                                                                        of references electronically on our                   the significance of the population
                                                as threatened or endangered under the
                                                                                                        NMFS Web site at http://                              segment to the remainder of the species
                                                Endangered Species Act (ESA). We have
                                                                                                        www.nmfs.noaa.gov/pr/species/                         (or subspecies) to which it belongs. As
                                                completed comprehensive status
                                                                                                        petition81.htm.                                       stated in the DPS Policy, Congress
                                                reviews for these two marine fish
                                                                                                                                                              expressed its expectation that the
                                                species in response to a petition                       FOR FURTHER INFORMATION CONTACT:                      Services would exercise authority with
                                                submitted by WildEarth Guardians.                       Ronald Salz, NMFS, Office of Protected                regard to DPSs sparingly and only when
                                                After reviewing the best scientific and                 Resources (OPR), (301) 427–8171 or                    the biological evidence indicates such
                                                commercial data available, we have                      Marta Nammack, NMFS, OPR, (301)                       action is warranted. Based on the
                                                determined that the gulf grouper is                     427–8403.                                             scientific information available, we
                                                currently in danger of extinction                       SUPPLEMENTARY INFORMATION:                            determined that the gulf grouper
                                                throughout its range and, therefore,                                                                          (Mycteroperca jordani) and the island
                                                meets the definition of an endangered                   Background
                                                                                                                                                              grouper (Mycteroperca fusca) are both
                                                species. After reviewing the best                          On July 15, 2013, we received a                    ‘‘species’’ under the ESA. There is
                                                scientific and commercial data                          petition from WildEarth Guardians to                  nothing in the scientific literature
                                                available, we have also determined that                 list 81 marine species or subpopulations              indicating that either of these species
                                                the island grouper is not currently in                  as threatened or endangered under the                 should be further divided into
                                                danger of extinction throughout all or a                Endangered Species Act (ESA). This                    subspecies or DPSs.
                                                significant portion of its range, but is                petition included species from many                      Section 3 of the ESA defines an
                                                likely to become so within the                          different taxonomic groups, and we                    endangered species as ‘‘any species
                                                foreseeable future. Therefore, we                       prepared our 90-day findings in batches               which is in danger of extinction
                                                conclude that the island grouper meets                  by taxonomic group. We found that the                 throughout all or a significant portion of
                                                the definition of a threatened species.
tkelley on DSK3SPTVN1PROD with PROPOSALS




                                                                                                        petitioned actions may be warranted for               its range’’ and a threatened species as
                                                We are soliciting information that may                  24 of the species and 3 of the                        one ‘‘which is likely to become an
                                                be relevant to inform the final                         subpopulations and announced the                      endangered species within the
                                                determinations for these two species.                   initiation of status reviews for each of              foreseeable future throughout all or a
                                                DATES: Comments on this proposed rule                   the 24 species and 3 subpopulations (78               significant portion of its range.’’ We
                                                must be received by November 23, 2015.                  FR 63941, October 25, 2013; 78 FR                     interpret an ‘‘endangered species’’ to be
                                                Public hearing requests must be made                    66675, November 6, 2013; 78 FR 69376,                 one that is presently in danger of
                                                by November 9, 2015.                                    November 19, 2013; 79 FR 9880,                        extinction. A ‘‘threatened species,’’ on


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                                                                  Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules                                         57315

                                                the other hand, is not presently in                     viability factors: Abundance, growth                  grouper with rounded preopercle and
                                                danger of extinction, but is likely to                  rate/productivity, spatial structure/                 moderate sized scales (Smith 1971).
                                                become so in the foreseeable future (that               connectivity, and diversity. These                    They have a comparatively elongated
                                                is, at a later time). In other words, the               viability factors reflect concepts that are           and compressed body shape with body
                                                primary statutory difference between a                  well-founded in conservation biology                  depth much less than their head length
                                                threatened and endangered species is                    and that individually and collectively                (Jenkins and Evermann 1889, Heemstra
                                                the timing of when a species may be in                  provide strong indicators of extinction               and Randall 1993). The dorsal fin has 11
                                                danger of extinction, either presently                  risk.                                                 spines and 16 to 17 rays, with the
                                                (endangered) or in the foreseeable future                  Scientific conclusions about the                   posterior margin rounded (Heemstra
                                                (threatened).                                           overall risk of extinction faced by the               and Randall 1993). The anal fin has 3
                                                   When we consider whether a species                   gulf grouper and the island grouper                   spines and 10 to 11 rays; and the gill
                                                might qualify as threatened under the                   under present conditions and in the                   rakers range from 21 to 26, not counting
                                                ESA, we must consider the meaning of                    foreseeable future are based on our                   rudiments (Heemstra and Randall 1993).
                                                the term ‘‘foreseeable future.’’ It is                  evaluation of the species’ demographic                Juvenile gulf grouper are greyish-brown
                                                appropriate to interpret ‘‘foreseeable                  risks and section 4(a)(1) threat factors.             with large, dark grey oblong blotches on
                                                future’’ as the horizon over which                      Our assessment of overall extinction                  the dorsal part of the body and fins
                                                predictions about the conservation                      risk considered the likelihood and                    (Heemstra and Randall 1993). Female
                                                status of the species can be reasonably                 contribution of each particular factor,               adults are generally dark brown to grey,
                                                relied upon. The foreseeable future                     synergies among contributing factors,                 but they can assume a juvenile pattern
                                                considers the life history of the species,              and the cumulative impact of all                      when disturbed or excited. Larger adult
                                                habitat characteristics, availability of                demographic risks and threats on the                  males develop a white margin along the
                                                data, particular threats, ability to predict            species.                                              pectoral fin, with the medial fin
                                                threats, and the reliability to forecast the               We then assess efforts being made to               developing a narrow white edge
                                                effects of these threats and future events              protect the species, to determine if these            (Heemstra and Randall 1993). In
                                                on the status of the species under                      conservation efforts are adequate to                  spawning aggregations, breeding
                                                consideration. Because a species may be                 mitigate the existing threats. Section                individuals exhibit conspicuous dark
                                                susceptible to a variety of threats for                 4(b)(1)(A) of the ESA requires the                    lines radiating from the eye (Sala et al.
                                                which different data are available, or                  Secretary, when making a listing                      2003). Gulf grouper can grow up to 150
                                                which operate across different time                     determination for a species, to take into             cm (in total length), 91 kg (in weight),
                                                scales, the foreseeable future is not                   consideration those efforts, if any, being            and 48 years (Heemstra and Randall
                                                necessarily reducible to a particular                   made by any State or foreign nation, or               1993, Aburto-Oropeza et al. 2008). Gulf
                                                number of years.                                        any political subdivision of a State or               grouper are considered voracious,
                                                   Section 4(a)(1) of the ESA requires us               foreign nation, to protect the species.               solitary predators, though little is
                                                to determine whether any species is                        Status reviews for the gulf grouper                known about their diet or feeding
                                                endangered or threatened due to any                     and the island grouper were conducted                 behavior.
                                                one or a combination of the following                   by NMFS OPR staff and an in-house
                                                five threat factors: The present or                     contractor. In order to complete the                  Reproductive Biology and Spawning
                                                threatened destruction, modification, or                status reviews, we compiled the best                  Behavior
                                                curtailment of its habitat or range;
                                                                                                        available information on the species’                    Gulf grouper are a protogynous
                                                overutilization for commercial,
                                                                                                        biology, ecology, life history, threats,              hermaphroditic fish, meaning they
                                                recreational, scientific, or educational
                                                                                                        and conservation status from                          mature as females and, later in life,
                                                purposes; disease or predation; the
                                                                                                        information contained in the petition,                transition into males. Gulf grouper
                                                inadequacy of existing regulatory
                                                                                                        our files, a comprehensive literature                 mature as females at an estimated six to
                                                mechanisms; or other natural or
                                                                                                        search, and consultation with experts.                seven years of age (Aburto-Oropeza et
                                                manmade factors affecting its continued
                                                                                                        We also considered information                        al. 2008). Gulf grouper are believed to
                                                existence. We are also required to make
                                                                                                        submitted by the public in response to                transition from female to male based
                                                listing determinations based solely on
                                                                                                        our petition findings. Draft status review            upon their size (size-advantage model)
                                                the best scientific and commercial data
                                                available, after conducting a review of                 reports were also submitted to                        (Bhandari et al. 2006, Zhou and Gui
                                                the species’ status and after taking into               independent peer reviewers; comments                  2010). The size-advantage model
                                                account efforts being made by any state                 and information received from peer                    theorizes that if it is advantageous for
                                                or foreign nation to protect the species.               reviewers were addressed and                          one sex to reproduce at a small size and
                                                   In assessing extinction risk of these                incorporated as appropriate before                    the other sex to reproduce at a larger
                                                two species, we considered the                          finalizing the draft reports. The gulf                size, then the individual should change
                                                demographic viability factors developed                 grouper and island grouper status                     sex at some point in life (Ghiselin 1969,
                                                by McElhany et al. (2000) and the risk                  review reports are available on our Web               Bhandari et al. 2006). Larger female
                                                matrix approach developed by                            site (see ADDRESSES section). Below we                grouper produce substantially more and
                                                Wainwright and Kope (1999) to organize                  summarize information from these                      higher quality eggs than smaller
                                                and summarize extinction risk                           reports and the status of each species.               females. Although not studied directly
                                                considerations. The approach of                         Status Reviews                                        in gulf grouper, an eight-year-old female
                                                considering demographic risk factors to                                                                       Mycteroperca produces approximately
                                                                                                        Gulf Grouper
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                                                help frame the consideration of                                                                               60 times the number of eggs that a five-
                                                extinction risk has been used in many                     The following section describes our                 year-old female produces (Aburto-
                                                of our status reviews (see http://                      analysis of the status of the gulf grouper,           Oropeza et al. 2008). For males, larger
                                                www.nmfs.noaa.gov/pr/species for links                  Mycteroperca jordani.                                 size is advantageous when competing
                                                to these reviews). In this approach, the                                                                      with other males for reproduction
                                                collective condition of individual                      Species Description                                   opportunities with females at spawning
                                                populations is considered at the species                  The gulf grouper (Jenkins and                       aggregation sites (Domeier and Colin
                                                level according to four demographic                     Evermann 1889) is a large, heavy-bodied               1997).


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                                                57316             Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules

                                                   Gulf grouper are transient aggregate                 grouper is considered restricted, defined             through 2012 throughout the species’
                                                spawners. Domeier and Colin (1997)                      as less than 800,000 km2 (Morris et al.               entire range. The El Club de Vuelos
                                                defined spawning aggregations as ‘‘a                    2000). Gulf grouper habitat                           boats fished at the Punta Lobos and San
                                                group of conspecific fish gathered for                  requirements vary throughout life.                    Bruno seamounts, both probable
                                                the purpose of spawning, with fish                      Groupers in general pass through a                    spawning aggregation sites at that time.
                                                densities or numbers significantly                      pelagic larvae phase (20–50 days)                     There are also anecdotal reports from
                                                higher than those found in the area of                  during which they settle into rocky,                  the 1940s and 1950s of fishermen using
                                                aggregation during the non-reproductive                 coastal reefs (Aburto-Oropeza et al.                  dynamite to capture large numbers of
                                                periods.’’ Spawning aggregations are                    2008). After this phase, they acquire                 gulf grouper at the San Bruno seamount
                                                further categorized as either ‘‘resident’’              juvenile characteristics while they settle            (Sáenz-Arroyo et al. 2005a). Sáenz-
                                                or ‘‘transient’’ depending upon                         into shallow, coastal habitats (e.g.                  Arroyo et al. (2005a) conducted over 30
                                                aggregation criteria. Transient spawning                Sargassum beds, seagrass areas,                       dives from 2001 through 2004 during
                                                aggregations typically (1) draw                         mangroves, and estuaries); this nursery               the gulf grouper spawning season at
                                                individuals from a relatively large area                stage can last up to two years. Adult gulf            sites that were recommended by the
                                                (individuals travel days to weeks to                    grouper predominately use rocky reefs                 original fishermen from El Club de
                                                gather), (2) occur during a very specific               and kelp beds of depths from five to 30               Vuelos. During these dives, only three
                                                time of year (one or two months), (3)                   meters (Heemstra and Randall 1993) and                gulf grouper were observed, all at the
                                                persist for only a few-day period, and                  deeper (30 to 45 m) during the summer                 Punta Lobos seamount. In 2002 and
                                                (4) do not occur year-round (Domeier                    (Moreno-Baéz 2010). During the                       2003, a biologist fished the San Bruno
                                                and Colin 1997). Transient aggregate                    spawning season, gulf grouper will                    seamount during the spawning
                                                species are often large sized predators                 aggregate in rocky reefs in depths from               aggregation season and was only able to
                                                that are not known to spawn outside of                  20 to 35 m (Sala et al. 2003).                        capture one gulf grouper (Sáenz-Arroyo
                                                aggregations (Domeier and Colin 1997).                     Historical and current gulf grouper                et al. 2005a). Since official Mexican
                                                   The location and timing of gulf                      population abundance is unknown.                      fishery landings data at the species level
                                                grouper spawning aggregations may                       Estimated trends in gulf grouper                      are only available since 2007, these data
                                                depend upon tidal influences on egg or                  abundance are based primarily on                      fail to encapsulate the major decline in
                                                larvae distribution (Domeier and Colin                  limited fisheries catch data and                      GOC gulf grouper abundance, which
                                                1997, Cherubin et al. 2011). All known                  anecdotal reports. The available                      likely started in the mid-20th century.
                                                spawning aggregation sites for gulf                     information indicates that gulf grouper
                                                grouper, current and historical, are                    were once a dominant species in rocky-                Summary of Factors Affecting the Gulf
                                                found in the Gulf of California (GOC)                   reef fish communities in terms of                     Grouper
                                                (Sala et al. 2004, Sáenz-Arroyo et al.                 biomass, before stocks collapsed in the                  Available information regarding
                                                2005a, Moreno-Baez 2010). The GOC,                      early 1970s (Sáenz-Arroyo et al. 2005a).             current, historical, and potential future
                                                with its length and combinations of                     In the 1930s, California fishermen                    threats to the gulf grouper was
                                                basins, islands, and sills, has large tides             reported gulf grouper as being abundant               thoroughly reviewed (Dennis 2015). We
                                                (up to 4 m) and fast tidal currents (up                 in Mexican waters between Bahı́a                      summarize information regarding
                                                to 1.5 m/sec) which peak during the full                Tortugas and Bahı́a Magdalena, and this               threats below according to three (out of
                                                moon (Filonov and Lavı́n 2003). Gulf                    species represented an important                      five) factors specified in section 4(a)(1)
                                                grouper are found on predictable                        component of the commercial fishery                   of the ESA: ‘‘Present or Threatened
                                                spawning aggregation locations before                   south of the U.S.-Mexico border                       Destruction, Modification, or
                                                and during the full moon in May (Sala                   (Croaker 1937, Fitch 1949). Combined                  Curtailment of its Habitat or Range’’;
                                                et al. 2004). Their spawning aggregation                landings of gulf grouper and broomtail                ‘‘Overutilization for Commercial,
                                                sites consist of rocky reef (gorgonians                 grouper for the California commercial                 Recreational, Scientific, or Educational
                                                and black coral) seamounts with abrupt                  fishery peaked in the early 1950s at 376              Purposes’’; and ‘‘Inadequacy of Existing
                                                relief habitat at 20 to 35 m depths. Adult              metric tons (mt), declined to around                  Regulatory Mechanisms.’’ We found
                                                gulf grouper form spawning                              100–150 mt between the late 1950s until               very little information regarding
                                                aggregations of 40 or more individuals                  the late 1960s, after which the grouper               potential threats that fall into the
                                                in areas larger than 1,000 m2 (Aburto-                  fishery completely crashed to near zero               section 4(a)(1) categories of either
                                                Oropeza et al. 2008). Based upon three                  landings by 1970 (California Department               ‘‘Disease and Predation’’ or ‘‘Other
                                                observed spawning aggregations, gulf                    of Fish and Wildlife—http://                          Natural or Manmade Factors.’’ These
                                                grouper spawning aggregation density                    libraries.ucsd.edu/apps/ceo/fishbull/).               subjects are data poor, but there are no
                                                was estimated at 220 fish/ha with fish                  In 1976, the California Department of                 serious or known concerns raised under
                                                sizes ranging from 100 to 150 cm total                  Fish and Game adopted no-take                         these threat categories with respect to
                                                length (Sala et al. 2003). Along the                    prohibitions for broomtail grouper and                gulf grouper extinction risk; therefore,
                                                Pacific coast, spawning aggregation sites               gulf grouper that are still in effect today.          we do not discuss these categories
                                                for gulf groupers are an unknown,                          In the GOC, gulf grouper accounted                 further here. See Dennis (2015) for
                                                though the size of the historical gulf                  for a significant proportion of the                   additional discussion of all ESA section
                                                grouper fisheries suggests that spawning                commercial landings weight in the mid-                4(a)(1) threat categories.
                                                aggregation sites may have been present.                20th century. In 1960, gulf grouper
                                                                                                        represented approximately 45 percent of               Present or Threatened Destruction,
                                                Population Structure, Distribution,                     the artisanal fishery in the GOC (Aburto-             Modification, or Curtailment of Its
                                                Abundance and Habitat                                                                                         Habitat or Range
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                                                                                                        Oropeza et al. 2008). Based on anecdotal
                                                  The gulf grouper resides in the                       accounts, boats from El Club de Vuelos                  Since the beginning of the 20th
                                                subtropical eastern Pacific Ocean and                   sport fishing resort in Loreto (Mexico)               century, human population growth and
                                                Gulf of California from 32.84° N. (La                   landed an estimated 63 mt of gulf                     development has resulted in the loss
                                                Jolla, California, United States) to 23.22°             grouper during a 2-month period in                    and degradation of coastal habitats
                                                N. (Mazatlán, Sinaloa, Mexico)                         1962 (Sáenz-Arroyo et al. 2005a). By                 throughout the gulf grouper’s range.
                                                (Heemstra and Randall 1993). The                        comparison, only an estimated 58 mt of                Continued loss or degradation of these
                                                overall range distribution for gulf                     gulf grouper were harvested from 2006                 habitats represents a potential threat to


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                                                                  Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules                                          57317

                                                the species. The terrestrial habitat                    unconsumed shrimp food, detritus,                     habitat (Lozano-Montes et al. 2008).
                                                surrounding the GOC is mostly arid to                   phytoplankton, zooplankton, and                       Development of the GOC region has
                                                semi-arid with rivers feeding the                       bacteria is flushed into the GOC through              resulted in more dredging activities
                                                estuaries and marine waters with                        discharge channels (Barraza-Guardado                  (Zamora-Arroyo et al. 2005) and
                                                sediments and fresh water. Originating                  et al. 2013). Shrimp farm effluents                   increased nutrient loading into the
                                                in these dry environments, the rivers                   contribute 10.2 percent of the nitrogen               marine ecosystem, resulting in algal
                                                and estuaries are of limited supply and                 and 3.3 percent of the phosphorus                     growth and hypoxic waters that can
                                                great importance. There are ten major                   inputs into the GOC (Miranda et al.                   degrade and kill coral (Kline et al.
                                                rivers that provide freshwater, sediment,               2009). Adding these organic materials                 2006). The effects of climate change can
                                                and nutrient inputs to the GOC. These                   into the marine habitat, which is already             lead to coral loss and degradation
                                                rivers have been extensively dammed,                    receiving effluents from other                        through bleaching and mortality events
                                                exploited for agricultural uses, and                    anthropogenic sources, deteriorates                   from elevated ocean temperatures, loss
                                                polluted from agricultural and urban                    water quality through oxygen depletion,               of structural integrity, and ocean
                                                runoff. As a result, the coastal habitats               light reduction, increased salinity,                  acidification. During the 1997–1998 El
                                                bordering the GOC have been reduced                     increased chlorophyll and bacteria                    Niño event, sea surface temperature
                                                and degraded, while nearshore                           levels, and changes in benthic                        anomalies of greater than 1.5 °C
                                                salinities, which ecosystems have                       macrofauna, resulting in possible                     occurred from July 1997 through
                                                evolved for, have changed. The Rı́o                     eutrophication (Páez-Osuna 2001,                     January 1998. Coral bleaching was
                                                Colorado is the largest watershed                       Barraza-Guardado et al. 2013). For                    extensive throughout the southern GOC:
                                                flowing into the GOC, representing over                 example, the Altata-Ensenada del                      Over 30 percent of live coral cover was
                                                two-thirds of the GOC’s watershed                       Pabellón lagoon receives effluent from               bleached, of which, nearly 70 percent
                                                acreage. Historically, 16.4 million acre-               shrimp farms, intensive agriculture (i.e.,            died within a few months (Bonilla
                                                feet of water flowed annually into the                  sugar cane), and sewage from local                    2001). Though the 1997–1998 coral
                                                GOC from the Rı́o Colorado (Goodfriend                  cities, leading to phytoplankton blooms,              bleaching event was related to El Niño,
                                                and Flessa 1997, Bureau of Reclamation                  anoxia, and fish kill events (Páez-Osuna             similar impacts may be expected in the
                                                2012). Today the river rarely flows to                  1999). The combined effects of shrimp                 future due to increasing ocean
                                                the GOC due to the cumulative effects                   farm effluents (and other sources of                  temperatures associated with climate
                                                of two large dam projects (Hoover Dam                   anthropogenic nutrient loading) with                  change.
                                                and Glen Canyon Dam) and major water                    climate change may result in an
                                                                                                                                                                 The impact of anthropogenic
                                                diversions. Increased anthropogenic                     increased incidence of hypoxia due to
                                                                                                                                                              activities on GOC marine habitats will
                                                nitrogen from sewage, agricultural, and                 enhanced ocean stratification, decreased
                                                                                                                                                              likely increase in the future based on
                                                shrimp farming sources are directly                     oxygen solubility, increased
                                                                                                                                                              projected human population growth and
                                                utilized by macroalgae, creating more                   metabolism, and increased production
                                                                                                                                                              development in this region. Population
                                                frequent blooms and corresponding                       of organic matter (Rabalais et al. 2009).
                                                                                                                                                              growth in the GOC region is expected to
                                                anoxia throughout coastal habitats in                   Shrimp farm effluents also typically
                                                                                                                                                              continue at a high rate with
                                                the GOC (Piñón-Gimate et al. 2009).                   contain antibiotics which are used in
                                                                                                        large quantities to preemptively treat                approximately 150,000 new residents
                                                Juvenile gulf grouper reside in these                                                                         per year (Source: http://
                                                coastal habitats (such as Sargassum and                 bacterial diseases (Kautsky et al. 2000).
                                                                                                           Effluents from agricultural areas and              www.conapo.gob.mx/es/CONAPO/
                                                seagrass beds, mangroves, and other                                                                           Proyecciones_Datos). The Mexican
                                                                                                        aquaculture facilities also contribute to
                                                kinds of estuary habitats) during the                                                                         federal government has placed a major
                                                                                                        harmful algal blooms in the GOC. Red
                                                first few years of life, and are                                                                              emphasis on tourism and trade
                                                                                                        tides, which are produced by a
                                                susceptible to these environmental                                                                            development throughout the GOC.
                                                                                                        planktonic dinoflagellate (Prorocentrum
                                                changes (Aburto-Oropeza et al. 2008).                                                                         Beginning in 2008, the first paved
                                                                                                        minimum), were first reported in the
                                                   Shrimp aquaculture began in the GOC                  GOC in 1990. Between 1990 and 2003,                   highway along the Sonoran GOC coast
                                                in the early 1980s. The production of                   13 red tide events occurred, with six                 was constructed from Puerto Peñasco to
                                                cultivated shrimp in the GOC has                        occurring in shrimp ponds and seven                   Mexicali (population 689,775) (Wilder
                                                increased tremendously over the past 30                 occurring near aquaculture and                        et al. 2012b). In Puerto Peñasco, the
                                                years: 35 mt in 1985; 15,867 mt in 1995;                agricultural areas (Sierra-Beltrán et al.            construction of a new marina with
                                                33,480 mt in 2000; and 125,609 mt in                    2005). Most recently, a red tide occurred             associated breakwaters and facilities for
                                                2009 (Gillett 2008, SEPESCA–BC Web                      in January 2015 near San Felipe, Baja                 cruise liners has started and is expected
                                                page http://www.sepescabc.gob.mx/x/                     California that resulted in fish, bird, and           to be completed in 2015. With improved
                                                estadisticas/). Shrimp farms can                        marine mammal mortalities.                            accessibility by land and sea, Puerto
                                                negatively impact gulf grouper through                     GOC reefs are predominantly rocky,                 Peñasco is currently undergoing a
                                                direct loss of habitat and through habitat              with a coral component in the south,                  construction boom, with two major
                                                degradation. The conversion of natural                  which shifts to kelp (brown algae) in the             resorts adding over 100,000 rooms via
                                                saltmarshes and mangrove forests into                   north (Squires 1959). Reef habitats                   hotels and condominiums along with
                                                shrimp farms can result in the direct                   support a wide diversity and high                     golf courses and 22 small-scale
                                                loss of nursery areas for juvenile gulf                 density of marine life, including gulf                desalination plants (Wilder et al.
                                                grouper (Páez-Osuna 2001). In the                      grouper, and are particularly sensitive to            2012b). Two hundred kilometers south
                                                northern GOC, an estimated 95 percent                   anthropogenic threats. Both direct (e.g.,             in Puerto Libertad, the Liberty Cove
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                                                of mangrove forests are impacted by                     fishing with dynamite, dredging) and                  resort has been approved for 60,000
                                                shrimp farms (Glenn et al. 2006). GOC                   indirect (e.g., anthropogenic nutrients,              dwellings, golf courses, a race track, and
                                                shrimp ponds stock between 60,000 to                    climate change) activities have had a                 a marina. Another project, the Escalera
                                                200,000 shrimp per hectare, and require                 detrimental impact on the reefs within                Náutica del Mar de Cortés y Riviera
                                                a daily water exchange of three to six                  the gulf grouper’s range. In the past,                Maya, will construct 29 new marinas
                                                percent (Páez-Osuna et al. 1998, Páez-                dynamite was often used for fishing on                throughout the GOC with facilities to
                                                Osuna et al. 2003). During water                        reefs, which has resulted in permanent                accommodate cruise ships and 60,000
                                                exchanges, organic matter from                          damage to gulf grouper spawning                       boats annually (Wilder et al. 2012b).


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                                                57318             Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules

                                                Another purpose of the improved ports                   groups are removed at a high rate,                    Sáenz-Arroyo et al. (2005a and 2005b)
                                                is to increase trade. For example, after                leading to decreased productivity of a                interviewed 108 fishermen from 11
                                                dredging its harbor in 2013, the Port of                population. In one study of the artisanal             fishing communities in the central GOC.
                                                Guaymas became the second largest                       fishery of Bahı́a de Los Angeles, nearly              Fishermen were asked to recall their
                                                Mexican port and is capable of handling                 99 percent of gulf grouper landed from                best day’s catch of gulf grouper, heaviest
                                                vessels up to 130,000 tons, while                       2002–2003 were immature fish (Aburto-                 fish caught, and years of these catches.
                                                increasing its port capacity from 8 to 30               Oropeza et al. 2008). These data suggest              For best day’s catch, catches decreased
                                                million tons of cargo.                                  that large, mature gulf grouper have                  significantly over time: 25 fish daily in
                                                   Increased development and                            been mostly removed from the                          the 1940s and 1950s; 10–12 fish daily in
                                                infrastructure will result in increased                 population.                                           the 1960s; and 1–2 fish daily in the
                                                energy and water needs. To meet these                      Spawning aggregations sites are                    1990s. For heaviest gulf grouper caught,
                                                needs there are plans to greatly expand                 particularly vulnerable to overfishing                weight per fish decreased significantly
                                                tidal power and desalination plant                      because they occur at predictable places              from ≥ 80 kg from the 1940s through the
                                                capacity in the region. The GOC is                      and times and they contain fish at a                  1960s to 60 kg by 2000. Among age
                                                considered one of the best tidal power                  much higher than normal density                       groups, 96 percent of the oldest (≥ 55
                                                locations in the world due to its large                 (Domeier and Colin 1997). Many                        years old) and 90 percent of the middle-
                                                tides and proximity to urban areas. Two                 fishermen base their fishing activities               aged (31–54 years old) fishermen had
                                                GOC tidal power site locations have                     upon the movement patterns of target                  captured gulf grouper, while only 45
                                                been identified and are in the early                    species, and knowledge of spawning                    percent of the young fishermen (15–30
                                                stages of planning: Bahı́a de Adair and                 aggregation sites is highly advantageous              years old) had. When asked whether or
                                                Canal del Infiernillo. Environmental                    (Sadovy et al. 1994, Moreno-Báez et al.              not they considered the gulf grouper
                                                impacts from tidal power include                        2012). Gulf grouper spawning                          depleted, 85 percent of the oldest
                                                habitat loss, increased turbidity,                      aggregation sites within the GOC (e.g.                considered them depleted, compared to
                                                mobilization of contaminants, and                       Punta Lobos and San Bruno seamounts)                  56 percent of the middle-aged, and 10
                                                changes in the morphodynamics of the                    have disappeared after periods of heavy               percent of the young fishermen (Sáenz-
                                                seabed (Gill 2005, Neill et al. 2009).                  exploitation (Sáenz-Arroyo et al. 2005a).            Arroyo et al. 2005a and 2005b). Sala et
                                                Plans for expanding tourism in the GOC                  The reduction or complete loss of                     al. (2004) interviewed 63 fishermen
                                                often include construction of                           additional spawning aggregations due to               (ages 25 to 67) from four fishing villages
                                                desalination plants (Wilder et al.                      overfishing represents a continued                    along the southern GOC. They found
                                                2012b). Desalination plants impact the                  threat to the gulf grouper.                           that the relative importance of gulf
                                                environment by both their very                             Commercial landings of gulf grouper                grouper as a target species and the
                                                substantial power requirements and the                  from the Pacific Ocean (U.S. vessels                  maximum size of gulf grouper caught
                                                wastewater discharges, which include                    fishing in Mexican waters) peaked in                  both declined markedly from the 1970s
                                                brine plumes (at twice the salinity of                  the early 1950s, followed by a                        to 2000.
                                                marine waters), antiscalents, coagulants,               population decline to near commercial                    Gulf grouper are highly prized by
                                                heavy metals, and membrane                              extinction by 1970. In 1976, California               recreational anglers, although data from
                                                preservatives that get released into the                declared the gulf grouper a prohibited                this fishery sector are sparse and the
                                                marine environment (Roberts et al.                      species. Based on recent fishery                      impact of recreational fishing on this
                                                2010). Marine organisms can also get                    independent surveys and fisheries data,               species is largely unknown. Based on
                                                trapped in desalination intake systems                  the gulf grouper is still considered a                anecdotal information, recreational
                                                (Wilder et al. 2012a). All of this                      very rare occurrence in the Pacific                   anglers caught large numbers of gulf
                                                increased development in and around                     Ocean.                                                grouper in the 1950s and 1960s and
                                                the GOC is anticipated to have negative                    Time series fisheries catch and effort             likely targeted known spawning
                                                effects on the GOC environment as a                     data available for gulf grouper in the                aggregation sites in the GOC (Sáenz-
                                                whole, and thus, on gulf grouper habitat                GOC are sparse. Official Mexican                      Arroyo et al. 2005a). During a two-
                                                within that environment.                                fisheries statistics did not include                  month period in 1962, anglers from El
                                                                                                        artisanal landings until 1988 (only                   Club de Vuelos sport fishing resort
                                                Overutilization for Commercial,                         commercial were included prior to that                harvested an estimated 63 mt of gulf
                                                Recreational, Scientific, or Educational                date), and species level information                  grouper (Sáenz-Arroyo et al. 2005a).
                                                Purposes                                                specific to gulf grouper are only                     More recently, Cudney-Bueno et al.
                                                   Gulf grouper are a highly prized                     available since 2007. Currently, gulf                 (2009) reported finding a large sport
                                                commercial and recreational fish                        grouper represent less than one percent               fishing derby targeting gulf grouper in
                                                species due to their large size and                     of the artisanal fishery in the GOC.                  2004 within the no-take zone of the
                                                palatability. Gulf grouper also exhibit                 However, recent gulf grouper landings                 Reserva de la Biosfera Isla San Pedro
                                                the following life history traits and                   can be misinterpreted, leading one to                 Martı́r.
                                                behavioral characteristics that increase                incorrectly conclude that the gulf                       In addition to overutilization by direct
                                                the species’ vulnerability to fishery                   grouper is a naturally rare species.                  harvest, gulf grouper are indirectly
                                                overutilization: Slow growth, late                      Anecdotal information based on Local                  harvested as bycatch in commercial
                                                maturation, large size, protogynous                     Fishermen Knowledge (LFK) indicates                   shrimp trawls (Ramı́rez et al. 2012) and
                                                hermaphroditism, long life-span, and                    that gulf grouper were once abundant in               illegal totoaba (Totoaba macdonaldi)
                                                the formation of transient spawning                     the GOC and represented approximately                 fisheries (Moreno-Báez et al. 2012). In
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                                                aggregations (Sadovy 1994). In                          45 percent of the artisanal fishery                   2012, commercial shrimp trawlers
                                                protogynous hermaphrodites, the largest                 landings weight in 1960 (Sáenz-Arroyo                harvested 42,310 mt of shrimp in the
                                                individuals are, in order, terminal                     et al. 2005a). Studies of LFK in the GOC              GOC. Mexican shrimp fisheries are not
                                                males, individuals undergoing sexual                    indicate sharp declines in gulf grouper               required to use bycatch reduction
                                                transition, and the largest, most fecund                abundance over the past 50 years (Sala                devices (BRDs), and recent studies
                                                females who are next in line for sexual                 et al. 2004, Sáenz-Arroyo et al. 2005a               estimated the bycatch ratio (bycatch:
                                                transition. Since fishers selectively                   and 2005b, Lozano-Montes et al. 2008,                 shrimp) at 6.1:1 (85.9 percent bycatch
                                                harvest the largest individuals, these                  and Moreno-Báez et al. 2010 and 2012).               rate; 2003–2009) in the central GOC


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                                                                  Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules                                         57319

                                                (Meltzer 2012) and 10.2:1 (91.1 percent                 covered by GOC MPAs are still actively                time (full moon in May), at known
                                                bycatch rate; 1992–2004) in the                         fished year-round with little or no                   locations (particular reefs and
                                                southern GOC (Madrid-Vera et al. 2007).                 regulations limiting harvest (Rodrı́guez-             seamounts), at higher than normal
                                                The totoaba, currently ESA-listed as                    Quiroz et al. 2010, Moreno-Báez et al.               densities. Some historical gulf grouper
                                                endangered, are currently harvested via                 2012). The lack of adequate enforcement               spawning aggregation sites have
                                                gill nets in the northern GOC for their                 is a chronic and pervasive problem for                completely disappeared following heavy
                                                swim bladders, which garner $8,500 per                  several MPAs within the GOC. For                      harvest (e.g. Punta Lobos and San Bruno
                                                kg (CIRVA 2014). Although it is                         example, one study of the Reserva de la               seamounts) (Sáenz-Arroyo et al. 2005a).
                                                unknown whether or not this totoaba                     Biosfera Isla San Pedro Martı́r,                      An analysis of 2002 and 2003 harvest
                                                fishery is also harvesting gulf grouper,                conducted from 2003 through 2008,                     data from Bahı́a de Los Angeles showed
                                                this fishery is currently using the same                found that 39 percent of the time sport               that 99 percent of the gulf grouper
                                                fishing ports (i.e., San Felipe, Golfo de               and commercial fishermen were fishing                 harvested were immature-sized fish,
                                                Santa Clara, and Puerto Peñasco) and                   in the 900 hectare core no-take zone,                 demonstrating the lack of reproductive
                                                harvest methods (i.e., gill nets) being                 including a large sport fishing derby                 age fish (Aburto-Oropeza et al. 2008).
                                                used to capture gulf grouper (Moreno-                   targeting gulf grouper in 2004 (Cudney-               Overall, the combination of high harvest
                                                Báez et al. 2012). Estimates of bycatch                Bueno et al. 2009).                                   rates at known spawning aggregation
                                                specific to gulf grouper in the GOC                        With the exception of the Parque                   sites and the trait of protogynous
                                                shrimp trawl fishery and the illegal                    Nacional Cabo Pulmo, fish species                     hermaphroditism significantly impacts
                                                totoaba fishery are not available.                      diversity and biomass have not                        gulf grouper productivity. Finally, gulf
                                                                                                        increased within designated GOC MPAs                  grouper have a small geographic range,
                                                Inadequacy of Existing Regulatory                       (Aburto-Oropeza et al. 2011). The
                                                Mechanisms                                                                                                    which may restrict their ability to move
                                                                                                        Parque Nacional Cabo Pulmo, located                   and adapt to environmental changes
                                                   In Mexico, the Comisión Nacional de                 on the southern tip of the Baja                       (Morris et al. 2000).
                                                Acuacultura y Pesca (CONAPESCA) has                     California peninsula, was established in
                                                the authority to implement fishing                                                                               Based upon the best available
                                                                                                        1995 to protect the large coral
                                                regulations (http://                                                                                          cumulative information from fisheries
                                                                                                        communities found there (Aburto-
                                                www.conapescasandiego.org/                                                                                    statistics, LFK, anecdotal reports, and
                                                                                                        Oropeza et al. 2011). The park includes
                                                contenido.cfm?cont=regulations), which                                                                        grey literature, we conclude that gulf
                                                                                                        a 2,501 hectare no-take reserve (35
                                                are enforced by the Mexican Navy.                                                                             grouper abundance has severely
                                                                                                        percent of the total park area). In a ten-
                                                Traditional fisheries regulations aimed                 year study, fish species richness and                 declined since the mid-20th century due
                                                at controlling catch and effort of gulf                 biomass significantly increased from                  primarily to direct harvest by
                                                grouper in Mexican waters are scarce.                   1999 to 2009, and previous studies have               commercial and artisanal fisheries (Sala
                                                Commercial fishing permits are only                     found gulf grouper inhabit park waters                et al. 2004, Sáenz-Arroyo et al. 2005a,
                                                available to Mexican nationals and                      (Aburto-Oropeza et al. 2011). The                     Aburto-Oropeza et al. 2008). The
                                                require a concession (either a                          conservation benefits of Cabo Pulmo are               primary signs of population decline are:
                                                cooperative or private business).                       threatened by development from the                    (1) Sharp reductions in harvest volumes,
                                                Commercial permits are awarded per                      tourist industry, as several large-scale              (2) significant decrease in average size
                                                vessel for two to five year durations and               resorts have recently been proposed for               and weight of harvested fish, (3)
                                                specify species (or species group)                      this area.                                            reduced spatial distribution and likely
                                                targeted, fishing area, and fishing                        In the U.S., the California Fish and               range contraction, and (4) extirpations
                                                method or gears. Recreational fishing is                Game Commission adopted a regulation                  or reductions of spawning aggregations
                                                allowed by national or foreign                          prohibiting the take or possession of                 (Sáenz-Arroyo et al. 2005a, Aburto-
                                                individuals through a single, non-                      gulf grouper in 1976 (Title 14, Section               Oropeza et al. 2008). In the GOC, gulf
                                                renewable, non-transferrable permit. In                 28.12). This regulation went into effect              grouper were once abundant and
                                                ocean waters and estuaries, a retention                 on March 1, 1977, and remains in effect               represented approximately 45 percent of
                                                limit of ten fish is allowed per angler                 today.                                                the artisanal fishery in 1960, but
                                                per day, of which only two can be gulf                                                                        declined to 10 percent by the 1970s, and
                                                                                                        Extinction Risk Assessment                            are now less than 1 percent of the
                                                grouper. Rubber-band, spring, or
                                                pneumatic harpoons are allowed during                     Gulf grouper are particularly                       fishery (Sáenz-Arroyo et al. 2005a). The
                                                recreational skin diving.                               susceptible to overfishing due to a                   sharp decrease in harvest levels since
                                                   Several marine protected areas                       combination of life history traits and                the 1970s was not due to decreased
                                                (MPAs) have been established in Mexico                  behavioral characteristics (Sadovy de                 fishing effort (fishing effort has
                                                within the gulf grouper’s range. MPAs                   Mitcheson et al. 2012). Biological                    generally increased) or new protective
                                                cover nearly one fifth of the GOC’s                     factors that likely increase the gulf                 regulations (which are of limited
                                                surface area, including 101,838 hectares                grouper’s intrinsic vulnerability to                  benefit), but rather was due to a decline
                                                designated as ‘‘no-take’’ areas (Aburto-                overfishing include large size, late onset            in gulf grouper abundance. Commercial
                                                Oropeza et al. 2011). Despite the                       of reproductive maturity, slow growth                 landings of gulf grouper from the Pacific
                                                establishment of multiple MPAs                          rate, and long life-span. As a                        Ocean (U.S. vessels fishing in Mexican
                                                throughout the GOC over the past few                    protogynous hermaphrodite, the gulf                   waters) peaked in the early 1950s,
                                                decades, overall protection of fisheries                grouper may be even more susceptible                  before the population declined to near
                                                resources is still inadequate for the                   to fishing which, through selective                   commercial extinction by 1970. Based
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                                                recovery of overexploited stocks. The                   removal of males, could reduce                        on recent fishery independent surveys
                                                lack of management plans, effective                     reproductive capacity. As a transient                 and fisheries data, the gulf grouper has
                                                regulations, and necessary resources to                 aggregate spawner, gulf grouper are                   not recovered and is still considered a
                                                operationalize and enforce MPAs in the                  highly susceptible to fishing                         very rare occurrence in the Pacific
                                                GOC significantly undermines their                      overutilization due to the predictability             Ocean portion of its range. Outside of a
                                                conservation benefits (Cudney-Bueno et                  of their locations in time and space.                 known population in Bahı́a Magdalena
                                                al. 2009, Rife et al. 2013, Cinti et al.                Once a year, adult gulf grouper                       (Octavio Aburto-Oropeza, Scripps
                                                2014). The large majority of the areas                  aggregate for reproduction at a known                 Institution of Oceanography, pers.


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                                                57320             Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules

                                                comm., 2014), there is no published                     Oropeza et al. 2008) and, due to the lack             commitment of funds for enforcement or
                                                evidence of gulf grouper still persisting               of protective regulations in Mexico (no               financial compensation of displaced
                                                along the Pacific coast of the Baja                     meaningful quotas nor protective                      fishermen. There are also large
                                                California peninsula. Current gulf                      regulations for gulf grouper), there is no            uncertainties associated with the
                                                grouper distribution appears to be much                 reason to expect fishing to be a                      effectiveness of the proposed enhanced
                                                more limited than their historical range                diminishing threat. Moreover, gulf                    enforcement measures given pervasive
                                                (Sáenz-Arroyo et al. 2005a). In the                    grouper are intrinsically vulnerable to               non-compliance with Mexican fisheries
                                                1930s, some irruptions of gulf groupers                 overfishing due to life history traits,               regulations and the economic incentives
                                                occurred along the San Diego coastline                  including large size, late onset of                   created by the extremely high valued
                                                (Hubbs 1948); but there are no records                  reproductive maturity, protogynous                    illegal totoaba fishery.
                                                of any occurring in this area since that                hermaphrodite life history, transient                    We did not identify any other
                                                time.                                                   aggregate spawning, slow growth rate,                 conservation efforts to protect and
                                                   In addition to direct harvest, other                 long life-span, and restricted geographic             recover gulf grouper that are either
                                                potential threats to gulf grouper                       range (Sadovy de Mitcheson et al. 2012).              underway but not yet fully
                                                abundance include bycatch in the                        Sharp decreases in harvest levels                     implemented, or are only planned. Our
                                                commercial shrimp and illegal totoaba                   observed since the 1970s are not due to               evaluation of the conservation efforts
                                                fisheries, habitat degradation and loss                 decreased fishing effort (fishing effort              identified lead us to conclude that
                                                from a variety of sources, and climate                  has generally increased) or new                       current conservation efforts cannot be
                                                change. However, there are no studies                   protective regulations (which are of                  considered effective measures for
                                                directly linking these factors to the                   limited benefit), but rather are due to a             significantly reducing the current gulf
                                                decline in gulf grouper abundance.                      decline in gulf grouper abundance.                    grouper extinction risk.
                                                Although the cumulative impact of                       Though a series of MPAs have been set
                                                these threats may be significant, the                                                                         Proposed Determination
                                                                                                        up in the GOC, only one, Cabo Pulmo,
                                                information available does not allow for                has an enforced no-take marine zone,                     Based on the best available scientific
                                                an accurate assessment of the relative                  and it is the only protected marine zone              and commercial information, as
                                                magnitude or contribution of these                      in the GOC that has seen improved                     summarized here and in Dennis (2015),
                                                threats to gulf grouper extinction risk.                marine fish life diversity and density                and consideration of efforts being made
                                                   Due to the inadequacy of existing                    over the past decade (Aburto-Oropeza et               to protect the species, we conclude that
                                                regulatory mechanisms, there is no                      al. 2011); therefore, the MPAs are not                the gulf grouper, Mycteroperca jordani,
                                                reason to expect the primary threat to                  anticipated to lead to a significant                  is currently at high risk of extinction
                                                gulf grouper from fisheries direct                      increase in gulf grouper abundance.                   throughout its range. We therefore
                                                harvest will diminish. Traditional                                                                            propose to list this species as
                                                fisheries regulations aimed at                          Protective Efforts                                    endangered under the ESA.
                                                controlling gulf grouper catch and                         In 2005, Mexico established the Área
                                                directed fishing effort in Mexican waters               de Refugio Vaquita Marina located in                  Island Grouper
                                                are very limited. While several MPAs                    the northern GOC to protect and                          The following section describes our
                                                have been established in the GOC in                     conserve the critically endangered                    analysis of the status of the island
                                                recent years, the lack of management                    vaquita (Phocoena sinus) by prohibiting               grouper, Mycteroperca fusca.
                                                plans, effective regulations, and                       gill net and trammel net use                          Species Description
                                                necessary resources to operationalize                   (SEMARNAT 2008). This prohibition is
                                                and enforce these MPAs significantly                    not directly designed to protect gulf                    The island grouper was first described
                                                undermines their conservation benefit                   grouper, but gill nets and trammel nets               under the name Serranus fuscus by
                                                (Cudney-Bueno et al. 2009, Rife et al.                  are two of the more common gulf                       Lowe (1836) based on specimens from
                                                2013, Cinti et al. 2014). With the                      grouper harvest methods, so the                       Madeira, Portugal. Diagnostic features of
                                                exception of the Parque Nacional Cabo                   prohibition could have the potential to               the island grouper include an oblong
                                                Pulmo, fish species diversity and                       benefit gulf grouper as well. However,                and compressed body with depth less
                                                biomass have not increased since the                    bycatch of vaquita in the illegal gill net            than head length, lower jaw extending
                                                establishment of GOC MPAs (Aburto-                      fishery for the endangered totoaba has                well in front of upper jaw, dorsal fin
                                                Oropeza et al. 2011). The conservation                  continued within this MPA after                       with 11 spines and 14–16 rays, anal fin
                                                benefits of Cabo Pulmo are currently                    implementation. In 2015, the Mexican                  with 3 spines and 10–12 rays with
                                                threatened by large-scale development                   federal government increased its efforts              rounded margin, and caudal-fin rear
                                                projects. Since 1976, the state of                      to protect vaquita by expanding the                   margin truncate (juveniles) to concave
                                                California has prohibited the take or                   Área de Refugio Vaquita Marina six-fold              (adults) (Heemstra and Randall 1993).
                                                possession of gulf grouper. However,                    to approximately 8,000 square                         Adults are brownish or dark grey, with
                                                this restriction only applies within                    kilometers. For the next two years, gill              irregular pale blotches and spots and a
                                                California waters, which represent a                    nets and long lines will be prohibited                prominent maxillary streak. Under
                                                very small portion of the species’                      within the MPA; and fishermen from                    stress this pattern may be reversed so
                                                historical range and may no longer be                   the nearby towns of San Felipe (Baja                  that the head and body are pale with
                                                part of the gulf grouper’s current range.               California, Mexico) and Golfo de Santa                irregular dark markings. Juveniles are
                                                Gulf grouper can still be harvested and                 Clara (Sonora, Mexico) will be                        mottled greenish-brown with prominent
                                                landed in Mexico by U.S. fishing                        financially compensated for changing                  white spots on head and body, white
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                                                vessels.                                                their harvest methods. Enforcement by                 streaks on median fins, with hyaline
                                                   The gulf grouper was once considered                 the Mexican Navy will be increased                    golden pectoral fins (Craig et al. 2011).
                                                abundant, but is now considered rare                    with the additional use of enforcement                The color pattern of mature females
                                                (Jenkins and Evermann 1889, Croker                      boats, light aircraft, and drones. These              from the Canary Islands suggests sexual
                                                1937, and Sáenz-Arroyo et al. 2005a).                  new conservation measures could result                dichromatism (i.e., males and females
                                                Direct harvest is the major reason for                  in decreased fishing pressure on gulf                 differ in color) (Bustos 2008). A large
                                                gulf grouper decline (Sala et al. 2004,                 grouper. However, these new measures                  proportion of sexually active females
                                                Sáenz-Arroyo et al. 2005a, Aburto-                     are temporary, and there is no long-term              have yellow pigmentation (dorsal fins


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                                                                  Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules                                          57321

                                                and/or chest, ventral or uniformly                      Consequently, the von Bertalanffy                     Population Structure, Distribution,
                                                throughout), while males are uniformly                  model typically does not describe the                 Abundance and Habitat
                                                brown (Bustos 2008). This species is                    growth of Mycteroperca spp. properly                     The island grouper is a subtropical
                                                also known to display a yellow (xanthic)                for the first few years of life, as                   species (40° N–10° N) that is endemic to
                                                color phase (Wirtz 2007), and a few                     evidenced by relatively large negative t0             volcanic archipelagos of Macaronesia:
                                                uniformly golden island grouper have                    values.                                               Canary Islands (Spain), Madeira and
                                                been reported from Madeira (Heemstra                       The island grouper is a nectobenthic               Azores (Portugal), and Cape Verde
                                                and Randall 1993).                                      (i.e., free-swimming, bottom oriented)                (Heemstra and Randall 1993). The
                                                   For many years island grouper were                   macrocarnivore that preys on fish,                    Canary Islands are located between 27°
                                                confused with another closely related                   crustaceans, and cephalopods                          and 29° N latitude and 13° and 18° W
                                                species, Mycteroperca rubra. Based                      (Harmelin-Vivien et al. 2001, Bustos                  longitude at a minimum distance of 100
                                                primarily on differences in gill raker                  2008). Island grouper are considered                  km and maximum distance of 450 km
                                                counts, Heemstra (1991) established that                mobile hunters and have been observed                 off the coast of Morocco. The Canary
                                                the species found in the Atlantic                       actively exploring their territories for              Islands archipelago is formed by seven
                                                Macaronesian region (from the Azores to                 prey (Bustos 2008).                                   main islands, with 1,379 km of
                                                Cape Verde) was M. fusca (with 20–24
                                                                                                        Reproductive Biology and Spawning                     coastline, a total land area of 7,447 km2,
                                                lower limb gill rakers), with the
                                                                                                        Behavior                                              and a human population size of
                                                distribution of M. rubra (with 28–31
                                                                                                                                                              approximately 2.1 million (Popescu and
                                                lower limb gill rakers) being limited to                   Bustos et al. (2010) studied the                   Ortega-Gras 2013). The Madeira
                                                the west coast of Africa and the                        pattern of sexual development and                     archipelago is located from 32° 37′ to
                                                Mediterranean Sea (Heemstra and                         reproductive characteristics of island
                                                Randall 1993).                                                                                                32° 52′ N latitude and 16° 39′ to 17° 15′
                                                                                                        grouper in the Canary Islands based on                W longitude, 754 km from the coast of
                                                   The island grouper is a slow-growing,
                                                                                                        samples of commercially harvested fish.               Africa and 964 km southwest of Lisbon.
                                                long-lived species which can attain
                                                                                                        Island grouper are a protogynous                      The archipelago consists of the two
                                                maximum sizes of at least 86 cm total
                                                                                                        hermaphroditic fish. Results of                       main inhabited islands (Madeira and
                                                length (TL) and 7.8 kg (Bustos 2008,
                                                                                                        histological analyses and demographic                 Porto Santo), with an estimated
                                                Bustos et al. 2010). Longevity of island
                                                                                                        structure suggest a monandric                         combined human population of
                                                grouper is estimated to be between 30
                                                                                                        protogynous sexual pattern, where                     268,000, and five uninhabited islands
                                                and 40 years (Bustos (2008, Bustos et al.
                                                                                                        males develop only through sex change                 (Desertas and Selvagens Islands). The
                                                2009). The instantaneous rate of natural
                                                                                                        (Bustos 2010). The length at which 50                 Madeira archipelago has 153 km of
                                                mortality estimated for island grouper is
                                                                                                        percent of the population reaches sexual              mostly rocky and steep coastline, and a
                                                between 0.146 and 0.158 per year
                                                (Bustos 2008). Island grouper length at                 maturity was estimated at 335 mm total                total land area of 801 km2. The Azores
                                                age was described by Bustos (2008) from                 length (TL), or about 4 years old. Of the             archipelago is located between 37° and
                                                commercial catches off Gran Canaria                     females over 398 mm TL (5–6 years old),               40° N latitude and 24° and 32° W
                                                and Fuerteventura (Canary Islands)                      95 percent were considered to be                      longitude, about 1,500 km west of
                                                between January 2004 and December                       mature. Island grouper sexual transition              Lisbon and 1,900 km southeast of
                                                2005. Von Bertalanffy growth model                      occurs between 428–725 mm TL, with                    Newfoundland. It is composed of nine
                                                parameters were as follows: L∞ = 898                    50 percent of females transformed into                islands and some small islets (Harmelin-
                                                mm; k = 0.062 per year; and t0 = ¥3.83                  males at around 678 mm TL (Bustos                     Vivien et al. 2001), with 667 km of
                                                years. Only 22 percent of the island                    2010). The presence of females in the                 coastline, a total land area of 2,333 km2,
                                                grouper sampled were older than ten                     larger size categories (up to 725 mm TL)              and a human population size of
                                                years, and the oldest fish in this study                implies that the conversion (female to                approximately 246,000. The Cape Verde
                                                was around 20 years old, 50 percent less                male) is not essential in all individuals.            archipelago is located between 14° and
                                                than the maximum age estimated by                       The overall sex ratio of males to females             17° N latitude and 22° and 25° W
                                                Bustos (2008). Significant differences                  (1:4.9) and the sex ratio of males to                 longitude, due west of Senegal, off the
                                                were found between males (n = 35) and                   mature females (1:3.4) were both                      west coast of Africa. It is composed of
                                                females (n = 153) for mean age (males                   significantly different from 1:1 (Bustos              ten islands (of which nine are inhabited)
                                                10.3 years versus females 7.1 years), L∞                2010).                                                and eight islets, with 1,020 km of
                                                (males 952 mm versus females 888 mm),                      In the Canary Islands, reproduction is             coastline, a total land area of 4,033 km2,
                                                and growth rate k (males 0.053 per year                 initiated in February, when water                     and a human population size of
                                                versus females 0.063 per year) (Bustos                  temperatures are around 18° C, and                    approximately 531,000. There are no
                                                2008).                                                  continues through August or September                 confirmed reports of island grouper off
                                                   While slow growth after the first few                when temperatures peak around 24–26                   the coast of West Africa, although
                                                years is typical for Mycteroperca, the                  °C (Bustos et al. 2010). The central                  ichthyofauna studies are lacking in this
                                                island grouper is particularly slow-                    period of spawning, as defined by                     region. One specimen was caught by a
                                                growing when compared to closely                        months when 50 percent or more of                     spearfisherman off Israel’s coast
                                                related species. On average, over 28                    females are in vitellogenesis (i.e., yolk             (Heemstra et al. 2010), but there are no
                                                percent of island grouper growth was                    deposition), is from April to July (Bustos            data confirming the existence of an
                                                achieved by the second year; by the                     et al. 2010). The formation of spawning               island grouper population in the
                                                fourth year this species attains lengths                aggregations is a common trait among                  Mediterranean.
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                                                of approximately half of the maximum                    groupers (Sadovy de Mitcheson et al.                     The island grouper is a demersal
                                                length observed. In general, growth                     2008). Although there are no published                species that is found predominantly
                                                within the genus Mycteroperca tends to                  studies on island grouper reproductive                near rocky or sandy-rocky sea-beds
                                                be faster in the early stages of life,                  behavior, spawning aggregations have                  (Heemstra and Randall 1993). Studies
                                                slowing down considerably in later                      been reported through personal                        have shown a positive correlation
                                                stages (Bullock and Murphy 1994,                        communication (J.P. Barreiros, UAC/                   between island grouper abundance and
                                                Manickchand-Heileman and Phillip                        IMAR in Rocha et al. 2008) from two                   structural complexity, algal cover
                                                2000, Strelcheck et al. 2003).                          locations in the Azores.                              (Bustos 2008), and upright seaweed


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                                                57322             Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules

                                                cover (Sangil et al. 2013b). The habitat                rare around Madeira Island, with the                  changes driven by overfishing, dynamite
                                                requirements of larval and juvenile                     possible exception of within the Garajau              fishing, physical alteration of the coast,
                                                island grouper are not well-studied. All                Marine Reserve (Ribeiro et al. 2005,                  pollution, the effects of global climate
                                                groupers pass through a pelagic larval                  Ribeiro 2008). Island grouper mean                    change, and the introduction of invasive
                                                phase, lasting between 20–50 days,                      densities were highly variable in studies             species.
                                                during which they can actively swim                     conducted around the Canary Islands.                     The island grouper is primarily found
                                                (Aburto-Oropeza et al. 2008). After the                 The highest mean densities were                       near the ocean bottom in areas with
                                                larval phase, groupers acquire juvenile                 reported around the lightly fished,                   high structural complexity (or
                                                characteristics during which they settle                remote island of El Hierro and within                 ‘‘roughness’’) and benthic cover (Bustos
                                                into shallow, coastal nursery habitats                  the designated marine reserves of La                  2008, Monteiro et al. 2008, Sangil et al.
                                                (e.g., Sargassum beds, seagrass areas,                  Graciosa (Chinijo Islands) and La Palma.              2013b). Canopy-forming macroalgae are
                                                mangroves, and estuaries); this nursery                 Island grouper were generally reported                a principal engineer organism on
                                                stage can last up to two years.                         as being very rare on the more populous               shallow rocky bottoms, providing the
                                                   The overall range distribution for                   and heavily fished Canary Islands of                  necessary habitat complexity and
                                                island grouper is considered restricted,                Gran Canaria and Tenerife.                            benthic cover to support and maintain
                                                defined as less than 800,000 km2                                                                              equilibrium of natural assemblages
                                                (Morris et al. 2000). The seafloor                      Summary of Factors Affecting the Island
                                                                                                        Grouper                                               (Hernández et al. 2008, Clemente et al.
                                                bathymetry around the Macaronesian                                                                            2010, Sangil et al. 2013b). Canopy-
                                                Islands is typically abrupt with a narrow                  Available information regarding
                                                                                                        current, historical, and potential future             forming macroalgae may also ameliorate
                                                contiguous shelf and a steep slope
                                                                                                        threats to the island grouper was                     the effects of a range of disturbances on
                                                plunging to depths of more than 1,000
                                                                                                        thoroughly reviewed (Salz 2015). We                   understory assemblages, thus enhancing
                                                meters. As a result, viable habitat for
                                                                                                        summarize information regarding                       the resistance of associated systems
                                                demersal species such as the island
                                                                                                        threats below according to three (out of              (Bertocci et al. 2014). The loss of
                                                grouper is considerably smaller than on
                                                                                                        five) factors specified in section 4(a)(1)            canopy-forming macroalgae, and
                                                continental shores, limiting the
                                                                                                        of the ESA: ‘‘Present or Threatened                   consequent increased environmental
                                                abundance of these populations (Diogo
                                                                                                        Destruction, Modification, or                         stress on associated organisms, could
                                                and Pereira 2013a, Popescu and Ortega-
                                                                                                        Curtailment of its Habitat or Range’’;                result in drastic reduction or local
                                                Gras 2013). Based on a wide range of
                                                                                                        ‘‘Overutilization for Commercial,                     extinction of understory species unable
                                                sources, Morris et al. (2000) classified
                                                the island grouper as having a ‘‘narrow                 Recreational, Scientific, or Educational              to survive harsh environmental
                                                depth range’’ defined as occurrence at                  Purposes’’; and ‘‘Inadequacy of Existing              conditions without the protective
                                                depths typically less than 20–30 m.                     Regulatory Mechanisms.’’ We found                     canopy (Bertocci et al. 2014). In the
                                                Although island grouper have                            very little information regarding                     Canary Islands, the natural balance
                                                occasionally been reported at greater                   potential threats under the section                   between seaweeds, herbivores, and
                                                depths (e.g., 50 m by Heemstra and                      4(a)(1) factors ‘‘Disease and Predation’’             predators has been disturbed due to the
                                                Randall 1993; 150 m by Bustos 2008;                     or ‘‘Other Natural or Manmade Factors.’’              fishing depletion of predators (e.g.,
                                                and 200 m by Craig et al. 2011), based                  These areas are data poor, but there are              sparids and labrids) of the sea urchin
                                                on the majority of observations, it is                  no serious or known concerns raised                   (Diadema africanum), the most
                                                assumed that their normal distribution                  under these threat categories with                    important herbivore of sublittoral rocky
                                                in the water column is at depths less                   respect to island grouper extinction risk;            bottoms (Hernández et al. 2008,
                                                than 30 m.                                              therefore, we do not discuss these                    Clemente et al. 2011). This has resulted
                                                   Historical and current island grouper                categories further here. See Salz (2015)              in an ecosystem imbalance whereby sea
                                                population abundance is unknown.                        for a more detailed discussion of all                 urchin populations have increased,
                                                Available information on island grouper                 ESA section 4(a)(1) threat categories.                while cover of upright seaweeds and
                                                distribution and abundance is primarily                                                                       canopy-forming macroalgae have
                                                                                                        Present or Threatened Destruction,                    decreased (Tuya et al. 2004, Hernandez
                                                from Underwater Visual Census (UVC)
                                                                                                        Modification, or Curtailment of Its                   et al. 2008, Clemente et al. 2011, Riera
                                                studies conducted at various locations
                                                                                                        Habitat or Range                                      et al. 2014). Seaweed beds have
                                                throughout the species’ range. There is
                                                a considerable amount of variation in                      Demersal fish populations around                   declined throughout much of the Canary
                                                island grouper mean densities reported                  volcanic islands may be particularly                  Islands archipelago and are now found
                                                in the literature. Island grouper were                  vulnerable to habitat related threats, as             in abundance only in restricted fishing
                                                reported as being very rare (0.03–0.10                  they are typically confined to a narrow               areas, remote islands, or areas where
                                                fish/100 m2) in two UVC studies of                      band within a few kilometers from shore               prevailing winds and currents limit
                                                benthic fish communities in the Azores                  due to the surrounding bathymetry.                    fishing pressure (Sangil et al. 2013b).
                                                (Harmelin-Vivien et al. 2001, Bertoncini                Various human activities throughout the               Steady declines in benthic cover of the
                                                et al. 2010). Compared to the Azores, a                 Macaronesian region can negatively                    canopy-forming brown macroalgae
                                                relatively higher mean density of island                impact near-shore, rocky marine                       (Fucus spiralis and Cystoseira spp.) in
                                                grouper (0.825 fish/100 m2) was                         habitats occupied by island grouper.                  the Canary Islands have been linked to
                                                reported from a single study in Cape                    Increased anthropogenic pressure on the               growing sea urchin populations in
                                                Verde (Freitas 2012). However, since                    more densely populated Macaronesian                   combination with rising sea surface
                                                sampling was conducted within the                       Islands (Madeira Island, and Tenerife                 temperatures (Hernández et al. 2008).
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                                                only operationalized MPA in Cape                        and Gran Canaria in the Canary Islands)               Population declines and increased
                                                Verde, on the uninhabited island of                     has resulted in continuous modification               fragmentation of the endemic red alga
                                                Santa Luzia (UNDP 2010), island                         and degradation of inshore habitats,                  (Gelidium canariense) have also been
                                                grouper mean density from this study                    placing new and unprecedented                         observed in Tenerife and Gran Canaria
                                                may not be representative of more                       demands on coastal marine resources                   during the last 20 years (Bouza et al.
                                                heavily fished areas throughout the                     (Hajagos and Van Tassell 2001, Ribeiro                2006). These studies suggest that, in
                                                archipelago. Based on limited                           2008). Potential threats to island                    addition to the direct impact of fishery
                                                information, island grouper appear to be                grouper habitat include ecosystem                     removals of island grouper, fishing can


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                                                                  Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules                                          57323

                                                initiate trophic cascades that may                      oceanographic conditions associated                   have already established in the port
                                                modify and degrade island grouper                       with climate change (combined with                    cities of Las Palmas and Santa Cruz
                                                habitats or preferred microhabitats.                    overfishing) have likely contributed to               (Riera et al. 2014). However, as with the
                                                   Large-scale coastal development                      the sea urchin population increase                    European sea bass, there are no studies
                                                began in the Canary Islands in the early                discussed above (Hernández et al.                    indicating that the invasive African
                                                1970s to meet the needs of a growing                    2010). In addition, Brito et al. (2005)               hind has negatively impacted native fish
                                                tourist industry (Hajagos and Van                       found 24 out of the 30 new records of                 populations.
                                                Tassell 2001). Similarly, the Madeira                   littoral bony fishes reported between
                                                Island coast has been extensively                                                                             Overutilization for Commercial,
                                                                                                        1991 and 2005 from two Canary Island
                                                armored and developed in the past two                                                                         Recreational, Scientific, or Educational
                                                                                                        marine reserves (La Graciosa in Chinijo
                                                decades (Ribeiro 2008). Artificial                                                                            Purposes
                                                                                                        Islands and La Restinga in El Hierro)
                                                harbors, marinas, beaches, ripraps,                     were species with tropical origins. The                  Island grouper are highly susceptible
                                                rubble mounds, and hotels were                          emergence of tropical species in                      to overfishing due to their limited range
                                                constructed on these islands, with few                  subtropical latitudes has also been                   and a combination of life history
                                                environmental precautions, resulting in                 reported in Madeira and the Azores                    characteristics including very slow
                                                massive alterations to the shoreline and                (Brito et al. 2005). However, the impact              growth, late maturation, large size, and
                                                siltation of nearshore benthic                          of progressive tropicalization of                     long life span (Bustos 2008, Bustos et al.
                                                communities (Hajagos and Van Tassell                    Macaronesian marine ecosystems on                     2009, Saavedra 2011, Diogo and Pereira
                                                2001). Baseline (pre-development)                       island grouper survival is widely                     2013a). Saavedra (2011) used a scale
                                                studies of the near-shore marine                        unknown.                                              developed by the Food and Agriculture
                                                communities in these heavily developed                     The introduction of invasive species               Organization (FAO) to characterize
                                                areas are lacking and, therefore, the                   through aquaculture poses a potential                 fishing vulnerability of target species in
                                                impacts of these habitat changes on                     threat to island grouper. Total                       the Canary Islands. Input parameters
                                                marine fish populations in general, and                 production of marine finfish in open-net              used for this scale included age at
                                                the island grouper in particular, are                   cages increased in the Canary Islands                 maturity, longevity, ratio of natural to
                                                largely unknown.                                        from 1,685 mt in 2001 to 7,900 mt in                  total mortality, growth rate, sexual
                                                   Pollution from a variety of sources                  2009 (APROMAR 2012). A massive                        strategy, and sex ratio. Island grouper
                                                also threatens marine ecosystems in the                 escape event occurred at an aquaculture               vulnerability was rated as either ‘‘high’’
                                                Macaronesian region. In the Canary                      operation on La Palma between                         or ‘‘very high’’ for all six parameters
                                                Islands, land-based sources of pollution                December 2009 and January 2010                        individually, and ‘‘very high’’ overall.
                                                include organic and inorganic                           resulting in the accidental release of 1.5            Certain behavioral traits, which are
                                                pollutants from developed areas and                     million fish (90 percent European sea                 common in groupers, may also add to
                                                farms (mainly banana and tomato), brine                 bass and 10 percent sea bream) into the               this species’ vulnerability to fishing.
                                                releases from desalination plants, and                  wild (Toledo-Guedes et al. 2014). As an               Territoriality, site specificity, and the
                                                thermal pollution from power plants                     opportunistic, high trophic level,                    formation of spawning aggregations
                                                (Riera et al. 2014). Other sources                      piscivorous species, non-native                       often result in groupers being an easy
                                                include nitrogenous waste from                          European sea bass could be competing                  target for fishermen (Randall and
                                                aquaculture, pollution derived from                     with native species such as the island                Heemstra 1991, Domeier and Colin
                                                ship traffic, and extraction of                         grouper (Toledo-Guedes et al. 2009).                  1997), although these traits have not
                                                construction materials from the seabed                  Toledo-Guedes et al. (2012) found                     been studied or well documented in the
                                                (Riera et al. 2014). In the Canary Islands,             evidence of gonadal maturation                        island grouper. Spawning aggregations,
                                                sharp declines in red alga (Gracilaria                  occurring in the wild in escaped male                 in particular, are highly vulnerable to
                                                cervicornis) coverage over the last 10                  and female European sea bass in the                   fishing due to their spatial and temporal
                                                years have been linked to coastal                       Canary Islands. The combination of                    predictability and to the large increase
                                                pollution from desalination plants and                  suitable biotic and non-biotic                        in catchability that often occurs when
                                                sewage from pipelines (Riera et al.                     conditions, high frequency of escape                  fish aggregate (Sadovy and Domeier
                                                2014). On the island of Madeira,                        events (Toledo-Guedes et al. 2009), and               2005). Although information on island
                                                pollution from raw sewage discharges,                   overutilization of native fish                        grouper spawning aggregations is
                                                sand mining, and sediment run-off                       assemblages (Tuya et al. 2006a) could                 lacking, there are documented examples
                                                severely decreases water clarity, which                 facilitate establishment of self-                     of sharp population declines resulting
                                                affects algae production (Ribeiro 2008).                reproducing non-native European sea                   from fisheries specifically targeting
                                                The direct impacts of different pollution               bass populations within the island                    aggregations of other grouper species
                                                sources on demersal fish populations in                 grouper’s range. However, studies                     (Colin 1992, Sala et al. 2001, Hamilton
                                                the Macaronesian region are not well-                   indicating that aquaculture escape                    and Matawai 2006, Sadovy de
                                                studied. The presence of continuous                     events have resulted in a decline in                  Mitcheson et al. 2012). The economic
                                                coastal currents around islands in this                 island grouper abundance are lacking.                 value of island grouper is also a factor
                                                region likely facilitates the dispersion of                The introduction of invasive species               that likely contributes to overutilization
                                                pollutants (Riera et al. 2014). Thus,                   through ship ballast water is also a                  of this species. The island grouper is
                                                while localized impacts may be acute                    potential threat to the island grouper.               highly prized by commercial and
                                                near highly concentrated point sources,                 Approximately 30,000 commercial                       artisanal fishermen for the quality of
                                                broader and long lasting impacts of                     vessels enter Canarian harbors each                   their flesh and typically fetch high
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                                                coastal pollution in this region have not               year, mostly in Gran Canaria and                      market prices (Heemstra and Randall
                                                been identified.                                        Tenerife (ISTAC 2013 in Riera et al.                  1993, Ribeiro 2008).
                                                   Certain changes are likely to occur in               2014). The African hind (Cephalopholis                   In protogynous hermaphrodites, such
                                                the world’s oceans due to long-term                     taeniops) is an invasive species from                 as the island grouper, the largest
                                                changes in global mean temperature and                  Guinea (West Africa) that is thought to               individuals are, in order, terminal
                                                possible anthropogenic impacts that                     have arrived in the Canary Islands in                 males, individuals undergoing sexual
                                                could pose potential future threats to                  ballast water (Riera et al. 2014). Stable             transition, and the largest females next
                                                island grouper habitats. Warmer                         populations of this predatory fish may                in line for sexual transition. Selective


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                                                57324             Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules

                                                removal of these groups at high rates                   1989–1999. Average monthly landings                   negative implications for the island
                                                can lead to decreased productivity of a                 (for months with data available) of                   grouper. Without effort data, it is not
                                                population. Island grouper may be                       island grouper were 46 fish. Detailed                 possible to say definitively that the
                                                particularly vulnerable to over-fishing                 monthly data were not available to                    decrease in landings is due to a decline
                                                due to the reduction in the species’                    assess trends in island grouper landings              in population abundance. However,
                                                potential reproductive capacity caused                  over time. Island grouper accounted for               total demersal species landings in the
                                                by the decrease in the number of males                  about 2.3 percent of the total catch in               Azores are consistently around 4,000 mt
                                                in the population (Huntsman and                         numbers of fish over this time period.                during the period when combined
                                                Schaaf 1994, Bustos et al. 2010). As the                Given their relatively large size and                 grouper landings declined
                                                relative numbers of terminal males fall,                market price, it is likely that the                   precipitously, which suggests that
                                                females may have difficulty finding a                   proportional contribution of island                   directed fishing effort for demersal
                                                terminal male to spawn with even if                     grouper to the landings weight and                    species did not decline.
                                                some remain (Hawkins and Roberts                        value in the Gran Canaria trap fishery is                The Cape Verde artisanal fishery
                                                2003). In addition, sexual transition                   considerably greater. Bustos et al. (2009)            typically lands between 4,000 mt and
                                                takes time and energy, including energy                 found very few island grouper greater                 5,000 mt of fish annually, of which
                                                expended on social interactions and                     than ten years old in commercial                      about 1,000 mt are demersal species
                                                competition among females vying for                     catches from Gran Canaria and                         (PRAO—CV 2012). Since 1992, the Cape
                                                dominance. Since removal of terminal                    Fuerteventura between January 2004                    Verde National Institute for Fisheries
                                                males by fishing will result in more                    and December 2005. For a species with                 Development (INDP) has compiled data
                                                sexual transitions, overall population                  a life-span between 30–40 years, these                on fishing catch and effort for the more
                                                fitness may be negatively impacted.                     results suggest that the island grouper is            important artisanal fishery target species
                                                                                                        experiencing a high rate of fishing                   (Medina et al. 2007). However, as a
                                                   Historical commercial and artisanal
                                                                                                        mortality in the more populated areas                 small component of the total catch,
                                                fisheries data are not available to
                                                                                                        within the Canary Islands archipelago.                island grouper are not one of the species
                                                evaluate long-term trends in island
                                                                                                           Island grouper are considered an                   monitored or reported in INDP official
                                                grouper landings, directed effort, or
                                                                                                        important component of the small                      statistics (Albertino Martins, personal
                                                catch rates over time. The limited
                                                                                                        artisanal fishery on El Hierro, where fish            communication). A recent assessment of
                                                landings data available for more recent
                                                                                                        traps are banned and demersal species                 mackerel scad (Decapterus macarellus),
                                                years indicate that island grouper are                  are mainly caught with hook-and-line                  bigeye scad (Selar crumenophthalmus),
                                                currently a very minor component of                     gears (Falcón et al. 2007a). Falcón et al.          and black spot picarel (Spicara
                                                commercial and artisanal fisheries                      (2007c) compared demersal species                     melanurus) indicates that stocks of
                                                throughout its range. The nearshore                     landings on El Hierro Island in the                   commercially important small pelagics
                                                demersal fishery in the Canary Islands                  period before and after implementation                are either fully exploited or
                                                is artisanal, consisting primarily of                   of the La Restinga Marine Reserve. From               overexploited in Cape Verde (DeAlteris
                                                small boats (Saavedra 2011). Fishing                    1990–1995 (before implementation) a                   2012). Continued overfishing of these
                                                methods used to catch demersal species                  total of 700 island grouper were landed               stocks could result in added fishing
                                                include hook and line, fish traps,                      (116.7 fish per year). From 1997–2005                 pressure on demersal species in Cape
                                                trammel nets, and gill nets (Bustos et al.              (after implementation) a total of 1,239               Verde. In Madeira, demersal species
                                                2009). Significant declines in                          island grouper were landed (137.7 fish                account for less than one percent of total
                                                populations of tunas and other pelagics                 per year). Over the entire period (1990–              fisheries landings (Morato 2012).
                                                since the 1970s have contributed to the                 2005), island grouper were the 9th most               Reported landings of island grouper in
                                                increased pressure on coastal demersal                  abundant species landed in numbers of                 Madeira are less than 1 mt per year for
                                                species (Moreno-Herrero 2011). In                       fish.                                                 all years from 2000–2013 (INE 2015).
                                                addition, in the 1980s the Moroccan                        In the Azores archipelago, the bottom                 Island grouper are also targeted in
                                                government restricted European Union                    longline and handline artisanal fishery               recreational and subsistence fisheries,
                                                vessel access to the Canary-Saharan                     for demersal species accounts for a                   and there are indications that these
                                                Bank fishing grounds, resulting in a                    significant portion of the total fishery              sectors are expanding rapidly in some
                                                shift in fishing effort by the Canary                   landings, and is by far the highest                   parts of the species’ range. Recreational
                                                artisanal fleet to coastal species                      valued fishery (Morato 2012). Annual                  fishing pressure has increased in the
                                                (Pascual-Fernandez and Diaz 1991 in                     landings by this fishery sector are                   past few decades as a direct result of
                                                Moreno-Herrero 2011). While landings                    consistently around 4,000 mt from 2000                human population growth and a
                                                volume of demersal species in the                       through 2010 (Morato 2012). By                        growing tourism sector (Sangil et al.
                                                Canary Islands are relatively small                     comparison, reported landings of island               2013b). For example, the number of
                                                compared to landings of pelagic species,                grouper for the Azores archipelago were               recreational spearfishing licenses sold
                                                these resources often have high                         less than 1 mt for every year from 2001–              in São Miguel Island (Azores) increased
                                                economic value (i.e., price per pound)                  2013 (INE 2015). Official data from the               from 138 in 1995 to 717 in 2011; and the
                                                as well as cultural value. In 2011,                     Portugal National Institute of Statistics             number of recreational fishing licenses
                                                demersal fish species accounted for 16.7                (INE) indicates a sharp and steady                    sold in the Canary Islands more than
                                                percent of the total fishery landings                   decline in combined ‘‘grouper’’ landings              doubled from 48,000 in 2005 to 116,000
                                                weight but 33.2 percent of the landing                  in the Azores from a high of 99 mt in                 in 2011 (Diogo and Pereira 2013a, Castro
                                                value in the Canary Islands (Popescu                    2003 to a low of 26 mt in 2013. The                   2014). There are also indications that
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                                                and Ortega-Gras 2013). Canary Islands                   combined grouper category includes                    Spain’s economic crisis and growing
                                                landings data prior to 2006 are only                    species of Epinephelus and                            unemployment have resulted in
                                                available from one port (Puerto de                      Mycteroperca. Although island grouper                 increased levels of subsistence fishing
                                                Mogan on Gran Canaria), and effort data                 landings account for a very minor                     and poaching in the Canary Islands
                                                are not available at all. Solari et al.                 component of combined grouper                         (Moreno-Herrero 2011). In Cape Verde,
                                                (2003) reported landings of island                      landings, this declining trend suggests               subsistence catches have shown an
                                                grouper in the multi-species trap fishery               that groupers, in general, are being                  increasing trend in recent years,
                                                from Puerto de Mogan for the period                     overfished, which would likely have                   suggesting increased dependence on


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                                                                  Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules                                          57325

                                                fish as a source of food, and possibly                  of island grouper in the recreational                 location of deployed fish traps, active
                                                related to declines in agricultural                     fishing survey is consistent with UVC                 fishing boats (commercial and
                                                production due to climate change                        studies indicating the rareness of this               recreational), shore based fishermen,
                                                induced droughts (Trindade-Santos et                    species in the Azores (Harmelin-Vivien                and spearfishermen. The following
                                                al. 2013).                                              et al. 2001, Bertoncini et al. 2010).                 biological parameters were used as
                                                   Recreational and subsistence fishery                    Without basic fisheries time series                indicators of conservation status:
                                                landings data are lacking, as there are no              data (e.g., catch, effort, sizes, and gears),         Percentage of seaweed cover; mean
                                                monitoring programs for these fishery                   it is difficult to quantitatively assess the          density of the sea urchin; mean biomass
                                                sectors throughout the Macaronesian                     impact of artisanal and recreational                  of sea urchin predators; mean biomass
                                                Islands. Jimenez-Alvarado (2010, in                     fishing on island grouper abundance. A                of combined grouper species (E.
                                                Saavedra 2011) estimated total                          few studies have demonstrated the                     marginatus, M. fusca, Serranus
                                                recreational fishery landings in the                    negative impact of fishing by correlating             atricauda); and mean biomass of the
                                                Canary Islands based on license sales by                relative fishing pressure with measures               Mediterranean parrotfish (Sparisoma
                                                fishing mode, number of recreational                    of island grouper abundance based on                  cretense), a highly prized fishing
                                                fishing vessels, and limited recreational               UVC sampling at different locations.                  resource and indicator of fish stock
                                                catch and effort survey data. Results                   Tuya et al. (2006a) found that, in the                status. Data were collected in 2009
                                                suggest that recreational fisheries have a              Canary Islands, island grouper mean                   using a UVC point-count method at 51
                                                significant impact on fish populations,                 density and mean biomass were                         sites (nine transects per site) around the
                                                and on three islands (Gran Canaria,                     significantly higher on islands with the              island. The correlation between fishing
                                                Gomera, and Fuerteventura) recreational                 lowest fishing pressure and lowest                    pressure and each biological parameter,
                                                landings of benthic-demersal species                    population density (El Hierro and                     including combined grouper biomass,
                                                likely exceed artisanal fishery landings.               Chinijo Islands) compared to other                    was high and negative. Sampled
                                                Although species level recreational                     islands within the archipelago. Similar               locations with the highest combined
                                                landings data are not available, this                   results were found for the dusky                      grouper mean biomass corresponded
                                                study indicates that the Canary Islands                 grouper, suggesting that human                        with areas of lowest fishing pressure—
                                                recreational fishery likely has an impact               intervention in the Canary Islands has                i.e., inside the La Palma MPA,
                                                on island grouper abundance.                            negatively impacted abundance of these                particularly within the no-take portion,
                                                   Diogo and Pereira (2013a) conducted                  large, slow growing species, with low                 where all fishing activity is prohibited.
                                                a characterization study of spearfishing                population turnover rates.                            The overall mean grouper biomass
                                                activity in Ponta Delgada, the capital of                  Tuya et al. (2006b) compared island                across all sites was 303.1 g/100 m2,
                                                São Miguel Island, the most populated                  grouper mean densities on El Hierro and               compared to 569.9 g/100 m2 within the
                                                island in the Azores archipelago. From                  the Chinijo Islands across sites with                 limited fishing MPA area, and 2,401.5 g/
                                                August 2001 through May 2002, they                      varying levels of protection from                     100 m2 within the no-take area. Grouper
                                                recorded data from 220 spearfishing                     fishing: RI = no-take zone; ZA = reserve              were virtually absent from the heavily
                                                trips (out of an estimated 281 total                    buffer zone, with only recreational                   fished areas just to the north of the MPA
                                                spearfishing trips taken). A total of nine              fishing allowed for grouper species; and              and on the eastern side of the island.
                                                island grouper were captured                            AV = outside reserve, with recreational               Although this study did not provide
                                                throughout the study period. By weight,                 and commercial fishing permitted,                     mean biomass data for groupers at the
                                                island grouper accounted for less than                  except fish traps, which are banned                   species level, island grouper accounted
                                                one percent of the total biomass of                     throughout these islands. A ‘‘reserve                 for approximately one-third of the total
                                                finfish captured with spear guns in the                 effect’’ (i.e., higher abundance within               biomass of the three grouper species
                                                survey. The mean length of island                       than outside the reserve boundary) was                combined (Sangil et al. 2013b).
                                                groupers captured (38 cm TL) was only                   not evident for island grouper within                    Ribeiro (2008) found higher density
                                                slightly larger than the size at first                  the El Hierro Restinga Reserve: i.e., no              and larger mean size of island grouper
                                                maturity. Results from this survey, in                  statistically significant differences were            within the protected Garajau Marine
                                                general, suggest that abundances of                     found in mean density between the no-                 Reserve (GMR) on Madeira Island
                                                species vulnerable to fishing (including                take zone, the buffer zone, and the                   compared to nearby unprotected areas
                                                island grouper) within the study site                   fishing area outside the reserve. A                   with similar habitat types. She
                                                have been significantly reduced due to                  ‘‘reserve effect’’ was found within the               attributed these differences to the
                                                heavy fishing pressure (Diogo and                       Chinijo Islands La Graciosa Reserve: i.e.,            regulations prohibiting all fishing in the
                                                Pereira 2013a).                                         island grouper mean densities were                    GMR. Before it was designated a marine
                                                   Diogo and Pereira (2013b) also                       statistically larger within the reserve               reserve, the GMR area was subjected to
                                                studied impacts of recreational boat                    (both RI and ZA zones) than in                        heavy fishing pressure from amateur
                                                fishing on demersal fish species off the                neighboring sites outside the reserve                 fishermen using explosives, gill nets,
                                                Azores islands of Faial and Pico from                   (AV zone). Bustos (2008) also found                   and spears (Ribeiro 2008).
                                                2004–2005. No island grouper catch                      evidence for a ‘‘reserve effect’’ within La
                                                were reported in a creel survey of 87                   Graciosa, and she observed no island                  Inadequacy of Existing Regulatory
                                                angler trips, and only 3 dusky grouper                  grouper in the two areas sampled                      Mechanisms
                                                (E. marginatus) were reported. Diogo                    outside the La Graciosa Reserve                          The nearshore demersal fisheries
                                                and Pereira (2013b) estimated the                       boundary.                                             throughout the Macaronesian Islands
                                                annual landings of all species by the                      Sangil et al. (2013a) studied the                  region are lightly regulated. Although
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                                                recreational boat fishery on these two                  relationship between fishing pressure                 these fisheries are primarily small-scale
                                                islands to be around 163 mt, which                      and conservation status at sites around               and artisanal, the cumulative impact on
                                                represents about 40 percent of the                      La Palma Island (Canary Islands).                     fish populations can be substantial,
                                                artisanal fishery landing weight in these               Fishing effort data were collected from               particularly for a species such as the
                                                areas. These results suggest that the                   boat-based and shore-based surveys                    island grouper, with a restricted range
                                                impact of the recreational boat fishery                 conducted twice per month for one full                and high vulnerability to
                                                on demersal fish communities in the                     year at fishing access sites around the               overexploitation. There are no
                                                Azores may be substantial. The absence                  island. Effort data included number and               commercial catch quotas, daily bag


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                                                57326             Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules

                                                limits, or seasonal closures in place for               There are also no MPAs or time-area                   and patchily distributed throughout the
                                                island grouper in any part of their range.              closures designed specifically to protect             species’ range. Typical of archipelago
                                                The Canary Islands is the only                          island grouper during spawning                        ecosystems, the Macaronesian Islands
                                                archipelago with a minimum size limit                   periods, and little is known about the                are highly fragmented, as geographic
                                                for this species, and enforcement does                  timing, location, or frequency of                     distances, bathymetry, and other
                                                not appear adequate to address non-                     spawning aggregations for this species.               physical factors result in various
                                                compliance with this regulation. Gear                                                                         degrees of isolation between islands and
                                                                                                        Extinction Risk Assessment
                                                restrictions (e.g., bans on fish traps, gill                                                                  local populations of demersal fish
                                                nets, bottom longlines, and SCUBA) are                     In determining an appropriate                      species (Medina et al. 2007). Given their
                                                in place for demersal fisheries in some                 foreseeable future timeframe for the                  geographic distribution and narrow
                                                areas and the use of explosives is widely               island grouper extinction risk                        depth ranges, it is likely that island
                                                prohibited. However, the effectiveness                  assessment, we considered both the life               grouper are inherently susceptible to
                                                of gear restrictions is substantially                   history of the species and whether we                 fragmentation, and this risk factor could
                                                reduced by inadequate enforcement, as                   could project the impact of threats or                be exacerbated by further population
                                                well as a shift in fishing effort to other              demographic risk factors through time.                declines. Because there is insufficient
                                                (legal) methods of capturing demersal                   We chose 40 years as the foreseeable                  information on genetic diversity, this
                                                species. There is some indication that                  future timeframe for island grouper.                  demographic viability criterion presents
                                                banning fish traps has had a positive                   Threats to island grouper can                         an unknown likelihood of contributing
                                                impact on island grouper abundance in                   potentially have long-lasting impacts,                to the island grouper’s extinction risk.
                                                the Canary Islands, although this ban                   given the species’ very slow growth rate,                The island grouper’s intrinsic
                                                only applies to two sparsely populated                  late maturation, and long maximum life                vulnerability to fishing is very high
                                                regions within the archipelago. Overall,                span. However, considering the limited                (Saavedra 2011, Diogo and Pereira
                                                it appears that current fishing                         information available to predict the                  2013a). Demographic viability risk
                                                regulations are inadequate for                          impacts from threats in the future, we                factors related to the island grouper’s
                                                addressing the direct threat to island                  felt 40 years was the most appropriate                growth rate, productivity, spatial
                                                grouper from fisheries overutilization.                 foreseeable future timeframe for island               structure, and range size all contribute
                                                Current regulations are also likely                     grouper.                                              to this species’ vulnerability to fishing
                                                                                                           Data from UVC sampling and fisheries               overexploitation (Bustos 2008, Bustos et
                                                inadequate to control overfishing of the
                                                                                                        landings indicate that the island grouper             al. 2009, Saavedra 2011, Diogo and
                                                main sea urchin predators, which, based
                                                                                                        is rare throughout much of its limited                Pereira 2013a). As a protogynous
                                                on recent studies from the Canary
                                                                                                        range and very rare in some areas                     hermaphrodite, the island grouper may
                                                Islands, has resulted in a trophic
                                                                                                        subjected to heavy fishing pressure. Of               be even more susceptible to fishing,
                                                cascade that has modified and degraded                  the 85 grouper species assessed by
                                                island grouper habitat.                                                                                       which, through selective removal of
                                                                                                        Morris et al. (2000), the island grouper              males, could reduce reproductive
                                                   In recent decades, no-take MPAs have                 was one out of only four species                      capacity (Huntsman and Schaaf 1994,
                                                received increased attention as a                       characterized as having both a                        Bustos et al. 2010). Certain behavioral
                                                conservation tool aimed at protecting                   ‘‘restricted’’ overall range and a                    traits (i.e., territoriality, site specificity,
                                                vulnerable fish populations (Halpern                    ‘‘narrow’’ depth range. Although there                and spawning aggregations), which are
                                                and Warner 2002). For some grouper                      are no population abundance estimates                 common among groupers, often result in
                                                species, increased fish density and size                available for island grouper, low and                 grouper species being an easy target for
                                                within no-take reserves may increase                    decreased density combined with a                     fishermen (Randall and Heemstra 1991,
                                                reproductive potential by promoting the                 highly restricted range indicate that                 Domeier and Colin 1997). Although not
                                                occurrence of spawning aggregations                     small population size is likely a risk                well-studied in the island grouper, these
                                                (Sanchez-Lizaso et al. 2000). The                       factor for this species, which could be               traits may add to the fishing
                                                ‘‘reserve effect’’ on island grouper                    disproportionally affected by coastal                 vulnerability of this species. The
                                                abundance (i.e., higher abundance                       development or a stochastic                           economic value of the island grouper is
                                                within than outside the reserve                         catastrophic event. Demographic                       also a factor that likely contributes to
                                                boundary) was reported for one reserve                  viability factors related to growth rate              overutilization of this species. Groupers
                                                on Madeira Island and two reserves in                   and productivity are also likely to                   are highly prized by commercial and
                                                the Canary Islands archipelago.                         contribute to the extinction risk based               artisanal fishermen for the quality of
                                                However, overall, the system of MPAs                    on the following island grouper life                  their flesh, and most species (including
                                                throughout the Macaronesian Islands is                  history characteristics: Slow growth,                 island grouper) fetch high market prices
                                                likely inadequate to protect island                     late maturation, low population                       (Heemstra and Randall 1993, Ribeiro
                                                grouper from the threat of fishing                      turnover rate, large size, and long life              2008).
                                                overutilization. No-take zones account                  span (Bustos 2008). While slow growth                    Historical fisheries data are not
                                                for only a small fraction of the total area             after the first few years is typical for              available to evaluate long-term trends in
                                                covered by MPAs within the island                       species of Mycteroperca, the island                   island grouper landings, directed effort,
                                                grouper’s range, as most areas still allow              grouper is one of the slowest growing                 or catch rates over time. The limited
                                                some types of fishing. In the Azores,                   species within this genus (Bustos et al.              commercial and artisanal catch data
                                                Madeira, and Canary Islands                             2009).                                                available indicate that, in recent years,
                                                archipelagos, there are only five no-take                  Although information on spatial                    island grouper landings have been
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                                                marine reserves, which occupy a total                   structure, connectivity, and dispersal                relatively small, and this species is
                                                area of 28 km2 (Fenberg et al. 2012).                   characteristics specific to island grouper            currently a very minor component of
                                                Given their small size and physical                     is sparse, it is somewhat likely that                 commercial and artisanal fisheries
                                                isolation from one another, no-take                     these factors represent a demographic                 throughout its range. The small
                                                zones may lack the connectivity to                      viability risk to this species. Island                contribution to recent fisheries landings
                                                allow the flow of larval and juvenile fish              grouper are rare in many areas studied,               is consistent with abundance
                                                across islands and archipelagos within                  and the few documented areas with                     information suggesting the island
                                                the region (Martı́n-Garcı́a et al. 2015).               relatively higher abundance are small                 grouper is generally a rare species.


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                                                                  Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules                                          57327

                                                Although fishing intensity is highly                    However, no-take zones account for                    connectivity. In addition, there is a
                                                variable between islands, there are                     only a small fraction of the total area               reasonable likelihood that the operative
                                                indications that artisanal fishing                      covered by MPAs within the island                     threats of fishing overutilization and the
                                                pressure for demersal species, in                       grouper’s range, as most MPAs still                   lack of adequate regulatory mechanisms
                                                general, is relatively high in many areas               allow some types of fishing. Given their              contribute significantly to the island
                                                throughout the island groupers’ range.                  small size, physical isolation from one               grouper’s risk of extinction.
                                                The depleted status of commercially                     another, and insufficient enforcement,
                                                                                                                                                              Protective Efforts
                                                important stocks of tunas and small                     the currently established marine
                                                pelagics in the Macaronesian region has                 reserves are likely inadequate to protect               We evaluated conservation efforts to
                                                also likely contributed to the increased                island grouper from the current and                   protect and recover island grouper that
                                                fishing pressure on coastal demersal                    future threat of fishing overutilization.             are either underway but not yet fully
                                                species in recent years (Moreno-Herrero                 Overall, we conclude that there is a                  implemented, or are only planned. As
                                                2011, DeAlteris 2012).                                  reasonable likelihood that the lack of                part of the European Union (EU), the
                                                   Several studies have demonstrated a                  adequate regulatory mechanisms and                    Azores, Madeira, and Canary Islands
                                                strong negative correlation between                     enforcement represent threats to the                  archipelagos are influenced by EU
                                                island grouper abundance and level of                   island grouper that contribute                        conservation initiatives and directives.
                                                fishing pressure (Tuya et al. 2006a,                    significantly to this species’ extinction             In 2008, the EU adopted the Marine
                                                Bustos 2008, Ribeiro 2008, Sangil et al.                risk.                                                 Strategy Framework Directive (MSFD)
                                                2013a, Sangil et al. 2013b). These                         Due to the species’ preferred depth                in order to achieve Good Environmental
                                                results suggest that fisheries                          range and the surrounding volcanic                    Status (GES) through ecosystem-based
                                                overexploitation has negatively                         island bathymetry, island grouper                     management in EU waters by 2020. To
                                                impacted island grouper abundance,                      habitat is typically confined to a narrow             comply with the MSFD, member states
                                                and some heavily fished areas have                      band within a few kilometers from                     must ensure that their biological and
                                                likely experienced a sharp decline. This                shore. Close proximity to the shore                   physical marine features adhere to the
                                                is particularly concerning for a rare                   increases the risk of habitat                         specific qualitative descriptors of GES
                                                species with a limited range and high                   modification from human activities                    for the maintenance of biological
                                                intrinsic vulnerability to the effects of               within the coastal zone, particularly on              diversity, habitat quality, and
                                                overfishing due to certain life history                 the more densely populated                            sustainable harvest levels of fish and
                                                and behavioral traits. The lack of                      Macaronesian Islands. Potential threats               shellfish stocks (Fenberg et al. 2012).
                                                baseline abundance information and a                    to island grouper habitat include:                    The establishment of a coherent
                                                time series of fishery dependent data,                  Declines in benthic cover (i.e., seaweeds             network of MPAs is the only mandated
                                                combined with limitations of the                        and macroalgae) due to overfishing of                 measure of the MSFD. The emphasis on
                                                available studies, make it difficult to                 key sea urchin predators; physical                    MPAs and biodiversity in the MSFD
                                                quantitatively assess the impact of this                alteration and armoring of the coast;                 reinforces previously established
                                                threat on island grouper abundance or                   destructive fishing practices; pollution;             commitments in the European
                                                species’ survival. However, based on the                and the effects of global climate change              Biodiversity Strategy and obligations
                                                cumulative information available, we                    (see section ‘‘Present or Threatened                  under the international Convention on
                                                conclude that there is a reasonable                     Destruction, Modification, or                         Biological Diversity (Bellas 2014). The
                                                likelihood that artisanal fishing                       Curtailment of Habitat or Range’’ for                 adoption of the EU’s MSFD policy
                                                overutilization contributes to the island               more details). While these ecosystem                  demonstrates a general willingness to
                                                grouper’s risk of extinction in a                       disturbances are well documented,                     achieve long-term protection of Europe’s
                                                significant way. There are also                         studies linking habitat related threats to            marine ecosystems, but whether the
                                                indications that rapidly expanding                      declines in island grouper abundance                  political will is strong enough in the
                                                recreational fisheries contribute                       are lacking. Although the cumulative                  Macaronesian Islands to achieve its
                                                significantly to the overutilization of                 impact of anthropogenic threats has                   objectives remains to be seen (Santos et
                                                island grouper in some parts of the                     likely modified some portion of the                   al. 2014).
                                                species’ range.                                         island grouper’s habitat, there is not                  The Portuguese government approved
                                                   Current fishing regulations designed                 enough scientific information available               two MSFD strategies in 2012, one for the
                                                to limit catch and effort are inadequate                to support a conclusion that habitat                  continental EEZ and one for the
                                                for addressing the direct threat to island              associated changes contribute to the                  extended continental shelf; but no
                                                grouper from fishing overutilization. In                extinction risk of this species in a                  MSFD strategy has yet been approved by
                                                general, there are few restrictions placed              significant way. The introduction of                  the autonomous governments of the
                                                on demersal fisheries throughout the                    invasive species from aquaculture                     Azores and Madeira archipelagos
                                                island grouper’s range. In areas where                  escape events and ship ballast water                  (Santos et al. 2014). In Spain, the MSFD
                                                regulations (e.g., size limits and gear                 also poses a potential threat to island               has resulted in passage of the 2010 Law
                                                restrictions) do exist, their effectiveness             grouper through increased competition                 on the Protection of the Marine
                                                is likely reduced by lack of enforcement                for limited resources (e.g., food, shelter)           Environment (LPME). The LPME
                                                and relatively high levels of non-                      and the possible spread of diseases and               provides a general legal framework for
                                                compliance. A well-designed system of                   parasites. However, as with habitat                   the conservation and sustainable use of
                                                no-take MPAs may be better suited than                  related threats, there is not enough                  marine resources, as well as specific
                                                traditional fishing regulations for                     scientific information available to                   language regarding the creation and
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                                                addressing the threat of fishing to highly              support a conclusion that threats related             management of a Spanish network of
                                                vulnerable, nearshore demersal species.                 to invasive species contribute to the                 MPAs, including some within the
                                                The ‘‘reserve effect’’ on island grouper                island grouper’s extinction risk in a                 Canary Islands (Bellas 2014). Four
                                                abundance (i.e., higher abundance                       significant way.                                      proposed Canary Islands MPAs are
                                                within than outside the reserve                            In summary, the island grouper                     currently waiting to be approved by the
                                                boundary) was reported for one reserve                  exhibits demographic risk factors                     Spanish government: One on the north
                                                on Madeira Island and two reserves in                   related to abundance, growth rate and                 coast of La Gomera, two in Tenerife, and
                                                the Canary Islands archipelago.                         productivity, and spatial structure and               one on the east coast of Gran Canaria


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                                                57328             Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules

                                                (Riera et al. 2014). However, previous                  (Planning and Management System for                   island grouper from fishing
                                                attempts to establish new MPAs in the                   Small Islands Protected Areas) is aimed               overutilization and inadequate
                                                Canary Islands have often been stalled                  at facilitating the development of                    regulatory mechanisms are likely to
                                                or abandoned due to stakeholder                         sustainable protected areas in the                    continue in the future, further
                                                opposition, political infeasibility, and                Azores through active involvement of                  exacerbating the demographic risk
                                                lack of funding (Chuenpagdee et al.                     stakeholders, promotion of economic                   factors associated with abundance,
                                                2013). For example, the regional island                 and cultural activities compatible with               growth rate and productivity, and
                                                government of Tenerife has been                         nature conservation, and innovative                   spatial structure and connectivity. We
                                                promoting the creation of MPAs on the                   planning and management of protected                  conclude that both the species’ current
                                                island since 2004. Two proposed MPAs                    areas at the island scale (Fonseca et al.             risk of extinction and the best available
                                                were finally approved in 2010—six                       2014).                                                information on the extent of, and trends
                                                years after initial planning started—but                   In summary, there are several                      in, the major threats affecting this
                                                to date neither one has been                            conservation initiatives that are either              species make it likely this species will
                                                implemented.                                            underway but not yet fully implemented                become an endangered species within
                                                   A joint United Nations Development                   or are still in the planning phase that               the foreseeable future (defined as 40
                                                Program (UNDP) and Global                               could potentially provide conservation                years) throughout its range. We
                                                Environment Facility (GEF) project                      benefits to the marine ecosystems                     therefore propose to list it as threatened
                                                titled ‘‘Consolidation of Cape Verde’s                  within the island grouper range.                      under the ESA.
                                                Protected Areas System’’ was initiated                  However, there are still major
                                                in 2010 in an effort to strengthen and                  uncertainties regarding whether or not                Effects of Listing
                                                expand Cape Verde’s national system of                  these initiatives will be fully                          Conservation measures provided for
                                                terrestrial and marine protected areas                  implemented, operationalized, and                     species listed as endangered or
                                                (UNDP 2013). Project objectives include:                adequately enforced. There are also                   threatened under the ESA include
                                                (1) Consolidation, expansion, and                       uncertainties associated with the                     recovery actions (16 U.S.C. 1533(f));
                                                operationalization of existing MPAs on                  effectiveness of these efforts in reducing            concurrent designation of critical
                                                the islands of Sal and Boavista for the                 the island grouper extinction risk.                   habitat, if prudent and determinable (16
                                                protection of fisheries resources, (2)                  Large-scale programs, such as the EU’s                U.S.C. 1533(a)(3)(A)); Federal agency
                                                building the national capacity for MPA                  MSFD, often have broad, general                       requirements to consult with NMFS
                                                management through new management                       objectives for improving marine                       under section 7 of the ESA to ensure
                                                sectors and authorities, and (3)                        stewardship which may or may not                      their actions do not jeopardize the
                                                promotion of participatory approaches                   include specific measures needed for                  species or result in adverse modification
                                                in the management and conservation of                   protecting a particular species at risk.              or destruction of critical habitat should
                                                the endemic biodiversity of Cape Verde.                 Regional, local and grassroots efforts                it be designated (16 U.S.C. 1536); and
                                                The project is expected to add 41,214 ha                may face fewer legal, political, and                  prohibitions on taking (16 U.S.C. 1538).
                                                of terrestrial and marine protected areas               social hurdles in terms of                            Recognition of the species’ plight
                                                (i.e., a 38 percent expansion over the                  implementation as compared to larger                  through listing promotes conservation
                                                existing baseline).                                     scale national programs. However,                     actions by Federal and state agencies,
                                                   Other regional, local and grassroots                 smaller scale programs, such as MAELs,                foreign entities, private groups, and
                                                efforts are underway to conserve and                    may be limited in their effectiveness for             individuals. The main effects of this
                                                protect marine resources in the                         species protection due to their small                 rule if finalized as proposed for gulf
                                                Macaronesian Islands. Local                             geographic size and inadequate                        grouper are prohibitions on take,
                                                nongovernmental organizations (NGOs)                    resources for long-term management                    including export, import, and use in
                                                and regional governments in the Canary                  and enforcement of conservation                       foreign commerce.
                                                Islands are promoting the creation of                   measures. We conclude that given large                Identifying Section 7 Conference and
                                                Micro Areas Ecoturı́sticas Litorales                    uncertainties associated with                         Consultation Requirements
                                                (MAELs). Due to their small scale,                      implementation, enforcement, and
                                                MAELs are less demanding on public                      effectiveness, the conservation efforts                  Section 7(a)(2) (16 U.S.C. 1536(a)(2))
                                                funding, typically less contentious, and                identified cannot be considered                       of the ESA and NMFS/USFWS
                                                follow a different legal model compared                 reasonably likely to significantly reduce             regulations require Federal agencies to
                                                to larger scale MPAs (Riera et al. 2014).               the current island grouper extinction                 consult with us to ensure that activities
                                                A well-designed and enforced network                    risk.                                                 they authorize, fund, or carry out are not
                                                of MAELs could provide additional                                                                             likely to jeopardize the continued
                                                conservation benefit to demersal fish                   Proposed Determination                                existence of listed species or destroy or
                                                populations in the Canary Islands. The                     Based on the best available scientific             adversely modify critical habitat.
                                                Canarias por una Costa Viva program is                  and commercial information, as                        Section 7(a)(4) (16 U.S.C. 1536(a)(4)) of
                                                a partnership among NGOs, universities,                 summarized here and in Salz (2015),                   the ESA and NMFS/USFWS regulations
                                                and local and regional governments.                     and consideration of protective efforts               also require Federal agencies to confer
                                                Costa Viva program objectives include                   being made to protect the species, we                 with us on actions likely to jeopardize
                                                studying the impacts of human                           find that the island grouper                          the continued existence of species
                                                population pressures on the coastal                     (Mycteroperca fusca) is at a moderate                 proposed for listing, or that result in the
                                                environment, increasing marine                          risk of extinction. The nature of the                 destruction or adverse modification of
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                                                environmental education and                             threats and demographic risks                         proposed critical habitat of those
                                                awareness, promoting and facilitating                   identified, taking into account the                   species. It is unlikely that listing the
                                                stakeholder involvement in marine                       uncertainty associated with the threats               gulf grouper under the ESA will
                                                resource management, and collaborating                  and risks, does not demonstrate the                   increase the number of section 7
                                                with government agencies in the                         species is presently in danger of                     consultations, because at present this
                                                sustainable use of Canary Islands                       extinction; and therefore, it does not                species is only known to occur outside
                                                marine resources. The Azores                            meet the definition of an endangered                  of the United States and is unlikely to
                                                University SMARTPARKS program                           species. However, the current threats to              be affected by Federal actions. Although


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                                                                  Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules                                          57329

                                                the gulf grouper’s historical range                     Identification of Those Activities That               will not be considered likely to result in
                                                includes parts of Southern California,                  Would Constitute a Violation of Section               a violation of section 9 of the ESA.
                                                there are no recent records indicating                  9 of the ESA                                          Although not binding, we are
                                                that this species still exists in U.S.                     On July 1, 1994, NMFS and FWS                      considering the following actions,
                                                waters.                                                 published a policy (59 FR 34272) that                 depending on the circumstances, as not
                                                Critical Habitat                                        requires us to identify, to the maximum               being prohibited by ESA section 9:
                                                                                                        extent practicable at the time a species                 (1) Take authorized by, and carried
                                                   Critical habitat is defined in section 3             is listed, those activities that would or             out in accordance with the terms and
                                                of the ESA (16 U.S.C. 1532(5)) as: (1)                  would not constitute a violation of                   conditions of, an ESA section
                                                Specific areas within the geographical                  section 9 of the ESA. Because we are                  10(a)(1)(A) permit issued by NMFS for
                                                area occupied by a species, at the time                 proposing to list the gulf grouper as                 purposes of scientific research or the
                                                it is listed in accordance with the ESA,                endangered, all of the prohibitions of                enhancement of the propagation or
                                                on which are found those physical or                    section 9(a)(1) of the ESA will apply to              survival of the species; and
                                                biological features (a) essential to the                this species. These include prohibitions
                                                conservation of the species and (b) that                                                                         (2) Continued possession of parts that
                                                                                                        against the import, export, use in foreign
                                                may require special management                                                                                were in possession at the time of listing.
                                                                                                        commerce, or ‘‘take’’ of the species.
                                                considerations or protection; and (2)                                                                         Such parts may be non-commercially
                                                                                                        These prohibitions apply to all persons
                                                specific areas outside the geographical                                                                       exported or imported; however the
                                                                                                        subject to the jurisdiction of the United
                                                area occupied by a species at the time                  States, including in the United States,               importer or exporter must be able to
                                                it is listed upon a determination that                  its territorial sea, or on the high seas.             provide evidence to show that the parts
                                                such areas are essential for the                        Take is defined as ‘‘to harass, harm,                 meet the criteria of ESA section 9(b)(1)
                                                conservation of the species.                            pursue, hunt, shoot, wound, kill, trap,               (i.e., held in a controlled environment at
                                                ‘‘Conservation’’ means the use of all                   capture, or collect, or to attempt to                 the time of listing, in a non-commercial
                                                methods and procedures needed to                        engage in any such conduct.’’ The intent              activity).
                                                bring the species to the point at which                 of this policy is to increase public                     Section 11(f) of the ESA gives NMFS
                                                listing under the ESA is no longer                      awareness of the effects of this listing on           authority to promulgate regulations that
                                                necessary. Section 4(a)(3)(A) of the ESA                proposed and ongoing activities within                may be appropriate to enforce the ESA.
                                                (16 U.S.C. 1533(a)(3)(A)) requires that,                the species’ range. Activities that we                NMFS may promulgate future
                                                to the extent prudent and determinable,                 believe could result in a violation of                regulations to regulate trade or holding
                                                critical habitat be designated                          section 9 prohibitions for this species               of gulf grouper, if necessary. NMFS will
                                                concurrently with the listing of a                      include, but are not limited to, the                  provide the public with the opportunity
                                                species. However, critical habitat shall                following:                                            to comment on future proposed
                                                not be designated in foreign countries or                  (1) Possessing, delivering,                        regulations.
                                                other areas outside U.S. jurisdiction (50               transporting, or shipping any individual
                                                CFR 424.12(h)). We can designate                        or part (dead or alive) taken in violation            Protective Regulations Under Section
                                                critical habitat in areas in the United                 of section 9(a)(1);                                   4(d) of the ESA
                                                States currently unoccupied by the                         (2) Delivering, receiving, carrying,
                                                species, if the area(s) are determined by                                                                        We are proposing to list the island
                                                                                                        transporting, or shipping in interstate or
                                                the Secretary to be essential for the                                                                         grouper as a threatened species. In the
                                                                                                        foreign commerce any individual or
                                                conservation of the species. Regulations                                                                      case of threatened species, ESA section
                                                                                                        part, in the course of a commercial
                                                at 50 CFR 424.12(e) specify that we shall                                                                     4(d) leaves it to the Secretary’s
                                                                                                        activity;
                                                designate as critical habitat areas                        (3) Selling or offering for sale in                discretion whether, and to what extent,
                                                outside the geographical range presently                interstate commerce any part, except                  to extend the section 9(a) ‘‘take’’
                                                occupied by the species only when the                   antique articles at least 100 years old;              prohibitions to the species, and
                                                designation limited to its present range                   (4) Importing or exporting any                     authorizes us to issue regulations
                                                would be inadequate to ensure the                       individual or part; and                               necessary and advisable for the
                                                conservation of the species.                               (5) Harming captive animals by,                    conservation of the species. Thus, we
                                                   The best available scientific and                    among other things, injuring or killing a             have flexibility under section 4(d) to
                                                commercial information does not                         captive animal, through experimental or               tailor protective regulations, taking into
                                                indicate that U.S. waters provide any                   potentially injurious care or conducting              account the effectiveness of available
                                                specific essential biological or physical               research or sexual breeding activities on             conservation measures. The 4(d)
                                                function for the gulf grouper. U.S.                     captive animals, outside the bounds of                protective regulations may prohibit,
                                                waters account for a very small portion                 normal animal husbandry practices.                    with respect to threatened species, some
                                                on the northern limit of the gulf                       Experimental or potentially injurious                 or all of the acts which section 9(a) of
                                                grouper’s historical range, and may no                  care or procedures and research or                    the ESA prohibits with respect to
                                                longer be part of the species’ current                  sexual breeding activities of gulf                    endangered species. These 9(a)
                                                range. Based on the best available                      grouper may, depending on the                         prohibitions apply to all individuals,
                                                information, we have not identified                     circumstances, be authorized under an                 organizations, and agencies subject to
                                                unoccupied areas in U.S. waters that are                ESA 10(a)(1)(A) permit for scientific                 U.S. jurisdiction. Since the island
                                                currently essential to the conservation                 research or the enhancement of the                    grouper occurs entirely outside of the
                                                of gulf grouper. Therefore, based on the                                                                      United States, and is not commercially
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                                                                                                        propagation or survival of the species.
                                                available information, we do not intend                                                                       traded with the United States, extending
                                                to designate critical habitat for gulf                  Identification of Those Activities That               the section 9(a) ‘‘take’’ prohibitions to
                                                grouper.                                                Would Not Constitute a Violation of                   this species will not result in added
                                                   The island grouper occurs entirely                   Section 9 of the ESA                                  conservation benefits or species
                                                outside of the United States. Therefore,                   We will identify, to the extent known              protection. Therefore, we do not intend
                                                we cannot designate critical habitat for                at the time of the final rule, specific               to issue section 4(d) regulations for the
                                                island grouper.                                         activities involving gulf grouper that                island grouper.


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                                                57330             Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules

                                                Public Comments Solicited                               NMFS/FWS policy (59 FR 34270; July 1,                 and that a Federalism assessment is not
                                                                                                        1994) requires us to solicit independent              required. In keeping with the intent of
                                                   To ensure that any final action
                                                                                                        expert review from qualified specialists,             the Administration and Congress to
                                                resulting from this proposed rule to list
                                                                                                        concurrent with the public comment                    provide continuing and meaningful
                                                two species will be as accurate and
                                                                                                        period. The intent of the peer review                 dialogue on issues of mutual state and
                                                effective as possible, we are soliciting
                                                                                                        policy is to ensure that listings are based           Federal interest, this proposed rule will
                                                comments and information from the
                                                                                                        on the best scientific and commercial                 be given to the relevant governmental
                                                public, other concerned governmental
                                                                                                        data available. We solicited and                      agencies in the countries in which these
                                                agencies, the scientific community,
                                                                                                        received peer review comments on each                 two species occur, and they will be
                                                industry, and any other interested
                                                                                                        of the status review reports, including               invited to comment. We will confer
                                                parties on information in the status
                                                                                                        from: three marine scientists with                    with the U.S. Department of State to
                                                review and proposed rule. Comments
                                                                                                        expertise on the gulf grouper, and three              ensure appropriate notice is given to
                                                are encouraged on these proposals (See                  marine scientists with expertise on the               foreign nations within the range of both
                                                DATES and ADDRESSES). We must base
                                                                                                        island grouper. Peer reviewer comments                species. As the process continues, we
                                                our final determination on the best                     for each species are incorporated into                intend to continue engaging in informal
                                                available scientific and commercial                     the draft status review reports and this              and formal contacts through the U.S.
                                                information when making listing                         12-month finding.                                     State Department, giving careful
                                                determinations. We cannot, for example,
                                                                                                        References                                            consideration to all written and oral
                                                consider the economic effects of a
                                                                                                                                                              comments received.
                                                listing determination. Final                              A complete list of the references used
                                                promulgation of any regulation(s) on                    in this proposed rule is available upon               List of Subjects
                                                these species’ listing proposals will take              request (see ADDRESSES).
                                                into consideration the comments and                                                                           50 CFR Part 223
                                                any additional information we receive,                  Classification                                          Endangered and threatened species,
                                                and such communications may lead to                     National Environmental Policy Act                     Exports, Transportation.
                                                a final regulation that differs from this
                                                proposal or result in a withdrawal of                     The 1982 amendments to the ESA, in                  50 CFR Part 224
                                                this listing proposal. We particularly                  section 4(b)(1)(A), restrict the
                                                                                                        information that may be considered                      Administrative practice and
                                                seek:                                                                                                         procedure, Endangered and threatened
                                                                                                        when assessing species for listing. Based
                                                   (1) Information concerning the threats                                                                     species, Exports, Imports, Reporting and
                                                                                                        on this limitation of criteria for a listing
                                                to either of the two species proposed for                                                                     recordkeeping requirements,
                                                                                                        decision and the opinion in Pacific
                                                listing;                                                                                                      Transportation.
                                                                                                        Legal Foundation v. Andrus, 675 F. 2d
                                                   (2) Taxonomic information on either
                                                                                                        825 (6th Cir. 1981), NMFS has                           Dated: September 14, 2015.
                                                of these species;
                                                                                                        concluded that ESA listing actions are                Samuel D. Rauch III,
                                                   (3) Biological information (life
                                                                                                        not subject to the environmental                      Deputy Assistant Administrator for
                                                history, genetics, population
                                                                                                        assessment requirements of the National               Regulatory Programs, National Marine
                                                connectivity, etc.) on either of these
                                                                                                        Environmental Policy Act (NEPA) (See                  Fisheries Service.
                                                species;
                                                                                                        NOAA Administrative Order 216–6).
                                                   (4) Efforts being made to protect either                                                                     For the reasons set out in the
                                                of these species throughout their current               Executive Order 12866, Regulatory                     preamble, 50 CFR parts 223 and 224 are
                                                ranges;                                                 Flexibility Act, and Paperwork                        proposed to be amended as follows:
                                                   (5) Information on the commercial                    Reduction Act
                                                trade of either of these species; and                      As noted in the Conference Report on               PART 223—THREATENED MARINE
                                                   (6) Historical and current distribution              the 1982 amendments to the ESA,                       AND ANADROMOUS SPECIES
                                                and abundance and trends for either of                  economic impacts cannot be considered                   1. The authority citation for part 223
                                                these species.                                          when assessing the status of a species.               continues to read as follows:
                                                   We request that all information be                   Therefore, the economic analysis
                                                accompanied by: (1) Supporting                          requirements of the Regulatory                           Authority: 16 U.S.C. 1531 1543; subpart B,
                                                documentation, such as maps,                                                                                  § 223.201–202 also issued under 16 U.S.C.
                                                                                                        Flexibility Act are not applicable to the
                                                                                                                                                              1361 et seq.; 16 U.S.C. 5503(d) for
                                                bibliographic references, or reprints of                listing process. In addition, this                    § 223.206(d)(9).
                                                pertinent publications; and (2) the                     proposed rule is exempt from review
                                                submitter’s name, address, and any                      under Executive Order 12866. This                        2. In § 223.102, in paragraph (e), the
                                                association, institution, or business that              proposed rule does not contain a                      table is amended by adding an entry for
                                                the person represents.                                  collection-of-information requirement                 ‘‘Grouper, island’’ under Fishes in
                                                Role of Peer Review                                     for the purposes of the Paperwork                     alphabetical order by common name to
                                                                                                        Reduction Act.                                        read as follows:
                                                  In December 2004, the Office of
                                                Management and Budget (OMB) issued                      Executive Order 13132, Federalism                     § 223.102 Enumeration of threatened
                                                a Final Information Quality Bulletin for                  In accordance with E.O. 13132, we                   marine and anadromous species.
                                                Peer Review establishing a minimum                      determined that this proposed rule does               *       *    *     *    *
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                                                peer review standard. Similarly, a joint                not have significant Federalism effects                   (e) * * *




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                                                                     Federal Register / Vol. 80, No. 184 / Wednesday, September 23, 2015 / Proposed Rules                                                          57331

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


                                                            *                            *                        *                      *                           *                       *                 *

                                                                                                                                      Fishes


                                                          *                              *                    *                      *                                 *                     *
                                                Grouper, island .............         Mycteroperca fusca ..... Entire species. .............          [Insert Federal Reg-                           NA                 NA
                                                                                                                                                         ister citation], 9/23/
                                                                                                                                                         2015.

                                                            *                             *                       *                          *                        *                      *
                                                  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).


                                                *       *       *       *         *                               Authority: 16 U.S.C. 1531–1543 and 16                     alphabetical order by common name to
                                                                                                                U.S.C. 1361 et seq.                                         read as follows:
                                                PART 224—ENDANGERED MARINE
                                                AND ANADROMOUS SPECIES                                             4. In § 224.101, in paragraph (h), the                   § 224.101 Enumeration of endangered
                                                                                                                table is amended by adding an entry for                     marine and anadromous species.
                                                  3. The authority citation for part 224                        ‘‘Grouper, gulf’’ under Fishes in                           *       *    *       *      *
                                                continues to read as follows:                                                                                                   (h) * * *

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


                                                            *                            *                        *                      *                           *                       *                 *

                                                                                                                                      Fishes


                                                         *                               *                    *                     *                                 *                      *                 *
                                                Grouper, gulf .................       Mycteroperca jordani ... Entire species ..............          [Insert Federal Reg-                           NA                 NA
                                                                                                                                                         ister citation], 9/23/
                                                                                                                                                         2015.

                                                            *                             *                       *                          *                        *                      *
                                                    1 Species
                                                            includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement, see 61 FR 4722, February 7,
                                                1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56 FR 58612, November 20, 1991).


                                                *       *       *       *         *
                                                [FR Doc. 2015–23502 Filed 9–22–15; 8:45 am]
                                                BILLING CODE 3510–22–P
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Document Created: 2015-12-15 09:45:16
Document Modified: 2015-12-15 09:45:16
CategoryRegulatory Information
CollectionFederal Register
sudoc ClassAE 2.7:
GS 4.107:
AE 2.106:
PublisherOffice of the Federal Register, National Archives and Records Administration
SectionProposed Rules
ActionProposed rule; 12-month findings; request for comments.
DatesComments on this proposed rule must be received by November 23, 2015. Public hearing requests must be made by November 9, 2015.
ContactRonald Salz, NMFS, Office of Protected Resources (OPR), (301) 427-8171 or Marta Nammack, NMFS, OPR, (301) 427- 8403.
FR Citation80 FR 57314 
RIN Number0648-XD97
CFR Citation50 CFR 223
50 CFR 224
CFR AssociatedEndangered and Threatened Species; Exports; Transportation; Administrative Practice and Procedure; Imports and Reporting and Recordkeeping Requirements

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