[Federal Register Volume 80, Number 234 (Monday, December 7, 2015)]
[Proposed Rules]
[Pages 76067-76115]
From the Federal Register Online via the Government Publishing Office [www.gpo.gov]
[FR Doc No: 2015-30660]



[[Page 76067]]

Vol. 80

Monday,

No. 234

December 7, 2015

Part II





Department of Commerce





-----------------------------------------------------------------------





National Oceanic and Atmospheric Administration





-----------------------------------------------------------------------





50 CFR Parts 223 and 224





Endangered and Threatened Wildlife and Plants; 12-Month Finding for 7 
Foreign Species of Elasmobranchs Under the Endangered Species Act; 
Proposed Rule

Federal Register / Vol. 80 , No. 234 / Monday, December 7, 2015 / 
Proposed Rules

[[Page 76068]]


-----------------------------------------------------------------------

DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

50 CFR Parts 223 and 224

[Docket No. 150909839-5839-01]
RIN 0648-XE184


Endangered and Threatened Wildlife and Plants; 12-Month Finding 
for 7 Foreign Species of Elasmobranchs Under the Endangered Species Act

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

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

-----------------------------------------------------------------------

SUMMARY: We, NMFS, have completed comprehensive status reviews under 
the Endangered Species Act (ESA) for seven foreign marine elasmobranch 
species in response to a petition to list those species. These seven 
species are the daggernose shark (Isogomphodon oxyrhynchus), Brazilian 
guitarfish (Rhinobatos horkelii), striped smoothhound shark (Mustelus 
fasciatus), narrownose smoothhound shark (Mustelus schmitti), spiny 
angel shark (Squatina guggenheim), Argentine angel shark (Squatina 
argentina), and graytail skate (Bathyraja griseocauda). Based on the 
best scientific and commercial information available, and after taking 
into account efforts being made to protect these species, we have 
determined that the daggernose shark (I. oxyrhynchus), Brazilian 
guitarfish (R. horkelii), striped smoothhound shark (Mustelus 
fasciatus), and Argentine angel shark (S. argentina) meet the 
definition of an endangered species under the ESA. We have determined 
that the narrownose smoothhound shark (M. schmitti) and spiny angel 
shark (S. guggenheim) meet the definition of a threatened species under 
the ESA. Therefore, we propose to list these six species under the ESA. 
Additionally, we have determined that the graytail skate (B. 
griseocauda) does not warrant listing under the ESA at this time. We 
are not proposing to designate critical habitat for any of the species 
proposed for listing because the geographical areas occupied by these 
species are entirely outside U.S. jurisdiction, and we have not 
identified any unoccupied areas within U.S. jurisdiction that are 
currently essential to the conservation of any of these species. We are 
soliciting comments on our proposal to list these six foreign marine 
elasmobranch species.

DATES: Comments on this proposed rule must be received by February 5, 
2016. Public hearing requests must be made by January 21, 2016.

ADDRESSES: You may submit comments on this document, identified by 
NOAA-NMFS-2015-0161, by either of the following methods:
     Electronic Submissions: Submit all electronic public 
comments via the Federal eRulemaking Portal. Go to www.regulations.gov/#!docketDetail;D=NOAA-NMFS-2015-0161. Click the ``Comment Now'' icon, 
complete the required fields, and enter or attach your comments.
     Mail: Submit written comments to 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 by NMFS. All comments received are a part of the 
public record and will generally be posted for public viewing on 
www.regulations.gov without change. All personally identifying 
information (e.g., name, address, etc.), confidential business 
information, or otherwise sensitive information submitted voluntarily 
by the sender will be publicly accessible. NMFS will accept anonymous 
comments (enter ``N/A'' in the required fields if you wish to remain 
anonymous).

You can find the petition, status review report, Federal Register 
notices, and the list of references electronically on our Web site at 
http://www.nmfs.noaa.gov/pr/species/petition81.htm.

FOR FURTHER INFORMATION CONTACT: Maggie Miller, NMFS, Office of 
Protected Resources (OPR), (301) 427-8403 or Chelsey Young, NMFS, OPR, 
(301) 427-8491.

SUPPLEMENTARY INFORMATION:

Background

    On July 15, 2013, we received a petition from WildEarth Guardians 
to list 81 marine species 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 27 of the 81 species and announced the initiation of 
status reviews for each of the 27 species (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 findings for 7 of those 27 species: daggernose 
shark (Isogomphodon oxyrhynchus), Brazilian guitarfish (Rhinobatos 
horkelii), striped smoothhound shark (Mustelus fasciatus), narrownose 
smoothhound shark (Mustelus schmitti), spiny angel shark (Squatina 
guggenheim), Argentine angel shark (Squatina argentina), and graytail 
skate (Bathyraja griseocauda). The status of, and relevant Federal 
Register notices for, the other 20 species 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 daggernose shark (I. 
oxyrhynchus), Brazilian guitarfish (R. horkelii), striped smoothhound 
shark (M. fasciatus), narrownose smoothhound shark (M. schmitti), spiny 
angel shark (S. guggenheim), Argentine angel shark (S. argentina), and 
graytail skate (B. griseocauda) are ``species'' under the ESA. There is 
nothing in the scientific literature indicating that any 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

[[Page 76069]]

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 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 of the following 
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. Under 
section (4)(b)(1)(A), 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.

Status Reviews

    Status reviews for the petitioned species addressed in this finding 
were conducted by a contractor for the NMFS Southeast Fisheries Science 
Center and are available at http://www.nmfs.noaa.gov/pr/species/petition81.htm or on the respective species pages found on the Office 
of Protected Resources Web site (http://www.nmfs.noaa.gov/pr/species/index.htm). These status reviews compiled information on each species' 
biology, ecology, life history, and threats from information contained 
in the petition, our files, a comprehensive literature search, and 
consultation with experts. The draft status review reports (Casselberry 
and Carlson 2015 a-g) were submitted to independent peer reviewers and 
comments and information received from peer reviewers were addressed 
and incorporated as appropriate before finalizing the draft report. The 
peer review report is available at http://www.cio.noaa.gov/services_programs/prplans/PRsummaries.html. These status reviews did 
not include extinction risk analyses for the species; thus, the 
extinction risk analyses for the seven species are included in this 12-
month finding. In addition to the status review reports, we considered 
information submitted by the public in response to our petition finding 
as well as information we compiled to assess the extinction risk of the 
species to make our determinations.

Extinction Risk Analyses

    We considered the best available information and applied 
professional judgment in evaluating the level of risk faced by each of 
the seven species. For each extinction risk analysis, we evaluated the 
species' demographic risks (demographic risk analysis), such as low 
abundance and productivity, and threats to the species including those 
related to the factors specified by the ESA section 4(a)(1)(A)-(E) 
(threats assessment), and then synthesized this information to estimate 
the extinction risk of the species (risk of extinction).
    The demographic risk analysis, mentioned above, is an assessment of 
the manifestation of past threats that have contributed to the species' 
current status and informs the consideration of the biological response 
of the species to present and future threats. For this analysis, we 
considered the demographic viability factors developed by McElhany et 
al. (2000). The approach of considering demographic risk factors to 
help frame the consideration of extinction risk has been used in many 
of our status reviews, including for Pacific salmonids, Pacific hake, 
walleye pollock, Pacific cod, Puget Sound rockfishes, Pacific herring, 
scalloped and great hammerhead sharks, and black abalone (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.
    In conducting the threats assessment, we identified and summarized 
the section 4(a)(1) factors that are currently operating on the species 
and their likely impact on the biological status of the species. We 
also looked for future threats (where the impact on the species has yet 
to be manifested) and considered the reliability to which we could 
forecast the effects of these threats and future events on the status 
of these species.
    Using the findings from the demographic risk analysis and threats 
assessment, we evaluated the overall extinction risk of the species. 
Because species-specific information (such as current abundance) is 
sparse, qualitative ``reference levels'' of risk were used to describe 
extinction risk. The definitions of the qualitative ``reference 
levels'' of extinction risk were as follows: ``Low Risk''--a species is 
at a low risk of extinction if it exhibits a trajectory indicating that 
it is unlikely to be at a moderate level of extinction risk in the 
foreseeable future (see description of ``Moderate Risk'' below). A 
species may be at low risk of extinction due to its present 
demographics (i.e., stable or increasing trends in abundance/population 
growth, spatial structure and connectivity, and/or diversity) with 
projected threats likely to have insignificant impacts on these 
demographic trends; ``Moderate Risk''--a species is at moderate risk of 
extinction if it exhibits a trajectory indicating that it will more 
likely than not be at a high level of extinction risk in the 
foreseeable future (see description of ``High Risk'' below). A species 
may be at moderate risk of extinction due to its present demographics 
(i.e., declining trends in abundance/population growth, spatial 
structure and connectivity, and/or diversity and resilience) and/or 
projected threats and its likely response to those threats; ``High 
Risk''--a species is at high risk of extinction when it is at or near a 
level of abundance, spatial structure and connectivity, and/or 
diversity that place its persistence in question. The demographics of 
the species may be strongly influenced by stochastic or depensatory 
processes. Similarly, a species may be at high risk of extinction if it 
faces clear and present threats (e.g., confinement to a small 
geographic area; imminent destruction,

[[Page 76070]]

modification, or curtailment of its habitat; or disease epidemic) that 
are likely to create such imminent demographic risks.
    Below we summarize information from the status review reports and 
information we compiled on the seven foreign marine elasmobranch 
species, analyze extinction risk of each species, assess protective 
efforts to determine if they are adequate to mitigate existing threats 
to each species, and propose determinations based on the status of each 
of the seven foreign marine elasmobranch species.

Daggernose Shark (Isogomphodon oxyrhynchus)

Species Description

    The daggernose shark (Isogomphodon oxyrhynchus) is the only species 
in the genus Isogomphodon, in the family Carcharhinidae (Compagno 
1988). It has a uniform gray or gray-brown color and white underside 
(Compagno 1984; Compagno 1988; Grace 2001), and is identified by its 
prominent, elongated snout. The pectoral fins of the species are very 
large and paddle-shaped (Compagno 1984; Compagno 1988; Grace 2001).

Range and Habitat Use

    The daggernose shark occurs in the central western Atlantic Ocean 
and Caribbean Sea and has been reported along the coasts of Venezuela, 
Trinidad, Guyana, Suriname, French Guiana, and northern Brazil (Lessa 
et al. 2006a). The Brazilian range includes the states of Amap[aacute], 
Par[aacute], and Maranh[atilde]o, with Tubar[atilde]o Bay in 
Maranh[atilde]o as its easternmost limit (Silva 2004; Lessa et al. 
1999a). The daggernose shark has one of the smallest ranges of any 
elasmobranch species (Lessa et al. 2000). It is a coastal species that 
is commonly found in estuaries and river mouths in tropical climates 
and is most abundant in these areas during the Amazonian summer (i.e., 
the rainy season) (Compagno 1984; Compagno 1988; Lessa 1997; Lessa et 
al. 1999a; Lessa et al. 2006b; Grace 2001). These sharks are often 
found in association with mangrove coastlines, occur in highly turbid 
waters and in low lying and indented coastlines that can have tide 
changes that vary as much as 7 meters (m) (Martins-Juras et al. 1987; 
Lessa et al. 1999a). Daggernose sharks occur in water depths between 8 
m and 40 m, temperatures ranging from 21.5 [deg]C to 31.5 [deg]C and 
salinities between 13.96 and 33.60 ppt (Lessa 1997; Lessa et al. 1999a, 
b). Salinity is considered a determining factor for the distribution of 
the species, but does not prevent the capture of daggernose sharks in 
shallow waters during the rainy season when waters are less saline 
(Lessa 1997). Specific winter habitats of the daggernose shark are 
unknown.

Diet and Feeding

    Little is known about the diet and feeding of the daggernose shark. 
Bigelow and Schroeder (1948) and Compagno (1984) suggest that they feed 
on schooling fishes, such as clupeids, sciaenids, herring, anchovies, 
and croakers. It is speculated that their small eyes and elongated 
snout emphasize the use of their rostral sense organs over eyesight 
when hunting in turbid waters (Compagno 1984). In Maraj[oacute] Bay in 
Brazil, daggernose sharks were found eating catfish (Family Ariidae) 
(Barthem 1985).

Growth and Reproduction

    Growth rates of daggernose sharks are similar between males and 
females, with an estimated growth rate from birth to age 1 calculated 
to be approximately 14 cm/year (Lessa et al. 2000). This rate then 
slows to approximately 10 cm/year from age 1 to 5-6 for males and age 1 
to 6-7 for females (Lessa et al. 2000). Thus, estimated ages at 
maturity are 5-6 years for males and 6-7 years for females. In terms of 
size, male daggernose sharks begin maturing between 90 cm and 110 cm 
total length (TL), with fully adult males observed at sizes larger than 
119 cm TL in the field (Lessa et al. 1999a). According to von 
Bertalanffy growth parameters, size at maturity is 103 cm TL for males 
and about 115 cm TL for females (Lessa et al. 2000), although the 
smallest pregnant female recorded was 118 cm long (Lessa et al. 1999a). 
After maturity is reached, growth rates decrease to less than 10 cm/
year (Lessa et al. 2000). Maximum age is estimated to be approximately 
20 years based on converting the length of a 160 cm TL female with 
parameters from the von Bertalanffy growth equation, although the 
largest male caught was 144 cm TL, corresponding to an age of 13 years 
old, and the oldest aged individuals from vertebrae analyses were of a 
7 year old male and a 12 year old female (Lessa et al. 2000).
    The reproductive cycle of daggernose sharks in Brazil is 
synchronized with the rain cycle. The rainy season runs from January to 
June and the dry season runs from July to December. A study by Lessa et 
al. (1999a) found that 70 percent of the pregnant females collected 
during the study in the rainy season were carrying a recently 
fertilized egg or very small embryo, suggesting that the ovulation 
period takes place at the end of the dry season or at the beginning of 
the rainy season (Barthem 1985). The gestation period is approximately 
12 months, with a protracted birthing period throughout the 6-month 
rainy season (Lessa et al. 1999a; Lessa et al. 2006b). Mature females 
captured with flaccid uteri and white follicles indicate that there is 
a break in follicle development between two successive pregnancies, 
which indicates a 2-year reproductive cycle (Lessa et al. 1999a). 
Mating and gestation periods can also be postponed to compensate for 
climate variability and changing environmental conditions across years 
(Lessa et al. 1999a). Female fecundity is low, commonly ranging between 
3 to 7 embryos per female, with the largest litter observed containing 
7 embryos, and one report of a female with 8 embryos (Bigelow and 
Schroeder 1948; Barthem 1985; Lessa et al. 1999a). There is no 
significant relationship between female size and litter size in 
daggernose sharks (Lessa et al. 1999a).

Genetics and Population Structure

    Studies examining the genetics of the species or information on its 
population structure could not be found.

Demography

    Based on the above life history parameters, and following methods 
in Cort[eacute]s (2002) for estimating survivorship, Casselberry and 
Carlson (2015a) estimated productivity (as intrinsic rate of population 
increase, ``r'') at 0.004 year-\1\ (median) within a range 
of -0.040-0.038 (5 percent and 95 percent percentiles) (Carlson 
unpublished). Median generation time was estimated at 10.6 years, the 
mean age of parents of offspring of a cohort ([micro]1) was 
10.7 years and the expected number of replacements (R0) was 
1.05. Lessa et al. (2010) estimated annual population growth to be r = 
-0.048 under natural mortality rates (of 0.28 using the Hoenig (1984) 
method and 0.378 using the Pauly (1980) method), and a generation time 
of 9 years. If fishing mortality rates were incorporated, the annual 
population growth was estimated to be r = -0.074, with a generation 
time of 8.4 years (Lessa et al. 2010). These demographic parameters 
place daggernose sharks towards the slow growing end of the ``fast-
slow'' continuum of population parameters calculated for 38 species of 
sharks by Cort[eacute]s (2002), which means this species generally has 
a low potential to recover from exploitation.

[[Page 76071]]

Historical and Current Distribution and Population Abundance

    In Brazil, daggernose sharks were historically found in the states 
of Amap[aacute], Par[aacute], and Maranh[atilde]o, and were first 
formally recorded in surveys from the 1960s in the state of 
Maranh[atilde]o (Lessa 1986). In 1999, daggernose sharks were 
documented as occurring in two Marine Conservation Areas in northern 
Brazil, the Parque Nacional Cabo Orange in Amap[aacute], and the 
Reentr[acirc]ncias Maranhenses in Maranh[atilde]o (Lessa et al. 1999b). 
However, in recent years, the absence of daggernose sharks in areas 
where they were previously common has been noted. For example, in the 
Bragan[ccedil]a fish market in northern Brazil (State of Par[aacute]), 
daggernose sharks were once among the most common shark species sold in 
the market. However, a genetic analysis of shark carcasses collected 
from this fish market between 2005 and 2006 found no evidence of 
daggernose sharks being sold in the market (Rodrigues-Filho et al. 
2009). Although the species' absence in fish markets could indicate 
obeyance of Brazilian law, which prohibited the catch of daggernose 
sharks in 2004, it has been noted that these laws are poorly enforced 
and frequently ignored (see discussion of Inadequacy of Existing 
Regulatory Mechanisms below). Additionally, while daggernose sharks 
were once caught abundantly in Maranh[atilde]o prior to 1992, they were 
notably absent in research surveys conducted from November 2006 to 
December 2007 (Almeida et al. 2011). Based on the species' life history 
parameters and rates of fishing mortality, population abundance was 
estimated to have declined by 18.4 percent per year for 10 years from 
the mid-1990s to mid-2000, resulting in a total population decline of 
over 90 percent (Santana and Lessa 2002; Rosa and Lima 2005; Kyne et 
al. 2012).
    Very little information is available on the distribution and 
abundance of the daggernose shark outside of Brazil. While undated 
catch records exist across the entire coastline of French Guiana, 
records are scarce throughout Suriname, Guyana, and Trinidad and Tobago 
(Bigelow and Schroeder 1948; Springer 1950; Compagno 1988; Global 
Biodiversity Information Facility (GBIF) 2013). Additionally, although 
Lessa et al. (1999a) includes Venezuela as part of the daggernose shark 
range (citing Cervig[oacute]n 1968), no other information could be 
found regarding the present existence of the daggernose shark in 
Venezuela. Given the species' sensitive biological traits to 
exploitation and evidence of high artisanal fishing pressure, it is 
assumed that dramatic population declines have occurred in the last 
decade throughout this part of the species' range, similar to the 
levels documented in Brazil, but scientific data on population trends 
are severely lacking for this region (Kyne et al. 2012).

Summary of Factors Affecting the Daggernose Shark

    We reviewed the best available information regarding historical, 
current, and potential threats to the daggernose shark species. We find 
that the main threat to this species is overutilization for commercial 
purposes. We consider the severity of this threat to be exacerbated by 
the species' natural biological vulnerability to overexploitation, 
which has led to significant declines in abundance and subsequent 
extirpations from areas where the species was once commonly found. We 
find current regulatory measures inadequate to protect the species from 
further overutilization. Hence, we identify these factors as additional 
threats contributing to the species' risk of extinction. We summarize 
information regarding these threats and their interactions below 
according to the factors specified in section 4(a)(1) of the ESA. 
Available information does not indicate that habitat destruction or 
modification, disease, predation or other natural or manmade factors 
are operative threats on these species; therefore, we do not discuss 
these factors further in this finding. See Casselbury and Carlson 
(2015a) for discussion of these ESA section 4(a)(1) threat categories.

Overutilization for Commercial, Recreational, Scientific, or 
Educational Purposes

    Based on historical catch data and trends, the primary threat to 
daggernose sharks is overutilization in artisanal fisheries. Given its 
rather shallow depth distribution, in Brazil, the species is bycaught 
in the artisanal gillnet fisheries for Spanish mackerel (Scomberomorus 
brasiliensis) and king weakfish (Cynoscion acoupa), which operate 
inside or near estuary mouths. Historically, the species was caught in 
large numbers along the northern Brazilian coastline and represented a 
significant component of the artisanal gillnet bycatch. For example, in 
the State of Par[aacute], daggernose sharks represented close to 70 
percent of the artisanal catch in the 1980s during the Amazonian summer 
(Lessa et al. 2010). Farther south, off the Maranh[atilde]o coast, 
harvest of daggernose sharks would begin in October and peak in 
January, with the catch per unit effort (CPUE) of these sharks in 
gillnets ranging from 6.04 kilogram (kg)/km/hour up to 71 kg/km/hour 
(during the peak in the rainy season) in the early 1990s. However, due 
to the species' sensitive life history traits, this high level of 
fishing mortality was found to be unsustainable, causing the daggernose 
shark population to decrease by 18.4 percent per year in the 1990s. By 
1999, the percentage of daggernose sharks in the artisanal gillnet 
bycatch along the Brazilian coast had significantly decreased, with 
daggernose sharks comprising only around 7-10 percent of the 
elasmobranch incidental catch (Lessa et al. 1999b; Lessa et al. 2000). 
By 2004 and 2006 the species was no longer observed or recorded in the 
states of Par[aacute] (Lessa et al. 2010) or Maranh[atilde]o (Almeida 
et al. 2011), respectively, based on data from research surveys 
conducted in these regions.
    Artisanal fisheries operating off Brazil continue to exert 
significant fishing pressure on the daggernose shark, which is likely 
contributing to fishing mortality rates that historically resulted in 
the substantial decline of the species. As such, overutilization 
continues to be a threat to the species as these fisheries are still 
highly active throughout its range. In fact, in the North region of 
Brazil (which includes the States of Amap[aacute] and Par[aacute]), the 
artisanal sector accounts for more than 80 percent of the total 
landings from this region and represents around 40 percent of the total 
artisanal landings for the entire country. These fisheries tend to be 
concentrated in areas where the daggernose shark would most likely 
occur, including the Amazon River estuary, small estuaries and bays, 
and shallow coastal waters within the extensive mangrove area that 
covers the northern coast of Brazil (Vasconcello et al. 2011). In the 
Northwest region of Brazil (which includes the States of 
Maranh[atilde]o south to Bahia), the artisanal sector is also the 
dominant fishing sector, accounting for more than 60 percent of the 
total landings from this region. The king weakfish fishery, which was 
noted as one of the main artisanal gillnet fisheries responsible for 
bycatching daggernose sharks, remains one of the most important 
fisheries in Brazil as evidenced by the fact that the species was the 
4th most landed marine fish in terms of volume in 2011 (21,074.2 t; 
Minist[eacute]rio da Pesca e Aquicultura (MPA) 2011). Together, the 
artisanal landings from these regions represent over 80 percent of the 
total artisanal landings for the entire country (Minist[eacute]rio do 
Meio Ambiente/Instituto Brasileiro do Meio Ambiente e dos

[[Page 76072]]

Recursos Naturais Renov[aacute]veis (MMA/IBAMA) 2007).
    These artisanal fishing practices and effort levels, which caused 
declines in daggernose shark populations off Brazil, are likely similar 
in Venezuela, Trinidad and Tobago, Guyana, Suriname, and French Guiana 
(which comprises the other half of the species' range). These countries 
have a substantial artisanal fishing sector presence, with catches from 
artisanal fishing comprising up to 80 percent of the total fish 
landings. In French Guiana, sharks alone comprised 40.4 percent of the 
annual artisanal landings for the local market (Harper et al. 2015). 
However, as noted in the Inadequacy of existing regulatory mechanisms 
section, due to minimal controls of these artisanal fisheries, 
including lack of enforcement capabilities of existing regulations, the 
available data indicate that many of these country's coastal marine 
resources are fully to overexploited (Food and Agriculture Organization 
of the United Nations (FAO) 2005a, 2005b, 2006, 2008). In Trinidad and 
Tobago, for example, it is estimated that the artisanal fleet catches 
between 75 and 80 percent of the total landings from these islands (FAO 
2006). Of concern, as it relates to overutilization of the daggernose 
shark, is the fact that Trinidad and Tobago have an open access fishery 
for the artisanal sector, which means there are no restrictions on the 
numbers and types of vessels, fishing gear, or trips (FAO 2006; 
Mohammed and Lindop 2015). In other words, any local vessel is allowed 
to enter the fishery and catch as much they can handle, with no 
restriction on fishing effort (FAO 2006). Similarly, Guyana also 
operates an open access fishery for its artisanal gillnet sector. Given 
that artisanal fishing for groundfish in Guyana, which comprises one of 
the country's two main fishing activities (the other being direct 
exploitation of shrimp by trawlers), is predominantly conducted using 
gillnets, open access fisheries cover a significant portion of the 
fishery sector for the country (FAO 2005a).
    As noted above, this essentially unregulated artisanal fishing 
throughout the Atlantic Caribbean, employing unselective net gear and 
concentrated in inshore coastal waters where daggernose sharks would 
primarily occur, has led to the overexploitation of many marine 
species, including sharks. However, there is virtually no information 
available on daggernose shark catches from the Caribbean countries in 
the daggernose shark range. These countries report general shark 
landings to the FAO but, in addition to these catches being 
significantly underestimated (on the order of 2.6 times for Trinidad 
and Tobago (Mohammed and Lindop 2015); 1.6 times for Guyana (Macdonald 
et al. 2015); 3.4 times for Suriname (Hornby et al. 2015); and 4 times 
for French Guiana (Harper et al. 2015)), daggernose sharks are not 
specifically identified in the catches (Shing 1999). However, 
historical and more recent information suggests daggernose sharks were 
and may still be utilized. Although the value of daggernose shark fins 
is low, its meat has been sold in markets from artisanal fisheries for 
decades (Lessa et al. 2006a), with Bigelow and Schroeder (1948) 
recording daggernose shark meat in markets in Trinidad and Tobago and 
noting its likelihood in markets in Guyana. Therefore, given the 
evidence of utilization of the species, as well as the significant 
fishing effort by artisanal fishing fleets throughout the daggernose 
shark range, including unregulated access to fishing grounds where the 
shark occurs, the observed absence of the daggernose shark in recent 
years can likely be attributed to overutilization of the species to the 
point where overutilization is significantly contributing to its risk 
of extinction.

Inadequacy of Existing Regulatory Mechanisms

    Throughout the species' range, species-specific protection for 
daggernose sharks is only found in Brazil. In 2004, the daggernose 
shark was first listed in Annex I of Brazil's endangered species list: 
``Lista Nacional Oficial de Esp[eacute]cies da Fauna Amea[ccedil]adas 
de Extin[ccedil][atilde]o--Peixes e Invertebrados Aqu[aacute]ticos'' 
(Silva 2004). An Annex I listing prohibits the catch of the species 
except for scientific purposes, which requires a special license from 
the Brazilian Institute of Environment and Renewable Resources (IBAMA) 
(Silva 2004). This protection was renewed in December 2014, when the 
daggernose shark was listed as ``critically endangered'' on the most 
recent version of the Brazilian endangered species list approved by the 
Ministry of the Environment (Directive No 445). ``Critically 
endangered'' on this list is defined as a species that presents an 
extremely high risk of extinction in the wild in the near future due to 
profound environmental changes or high reduction in population, or 
significant decrease in the taxon's range. In addition to the landing 
prohibition, daggernose sharks also receive protection when they occur 
within two of Brazil's marine protected areas (MPAs): The Parque 
Nacional Cabo Orange and the Reentr[acirc]ncias Maranhenses (Lessa et 
al. 1999b); however, the last time they were reported in these areas 
was in 1999.
    Although Brazil has a number of regulations in place to protect 
endangered or threatened species, like the ones described above for 
daggernose sharks, it is generally recognized that these regulations 
are poorly enforced, particularly within artisanal fisheries (Lessa et 
al. 1999b; Amaral and Jablonski 2005; Almeida et al. 2011; Rodrigues-
Filho et al. 2012). Poverty, lack of education within the artisanal 
fisheries sector, and increased artisanal fishing effort, especially in 
the State of Maranh[atilde]o, have already contributed to the decline 
of many elasmobranch populations, including the daggernose shark (Lessa 
et al. 1999b), despite the existence of protective legislation and 
marine protected areas. As such, effective conservation appears to be 
lacking in Brazil (Lessa et al. 1999b; Amaral and Jablonski 2005), with 
existing regulatory mechanisms likely inadequate to protect the 
daggernose shark from further fishery-related mortality.
    In December 2014, the Brazilian Government's Chico Mendes Institute 
for Biodiversity Conservation approved an FAO National Plan of Action 
(NPOA) for the conservation of sharks (hereafter referred to as FAO 
NPOA-sharks) for Brazil (No. 125). The plan considers the daggernose 
shark to be one of the country's 12 species of concern and recommends a 
moratorium on fishing with the prohibition of sales until there is 
scientific evidence in support of recovery (Lessa et al. 2005). 
Additionally, it proposes the expansion of the Reentr[acirc]ncias 
Maranhenses (where daggernose sharks were observed in 1999) to include 
the marine coastal zone and banks, providing additional protection to 
the sharks from potential fishery-related mortality. The plan 
recommends increased effort monitoring of vessels using nets in the 
area and increased education to encourage the release of live 
daggernose sharks and prevent the landing of the species. In general 
the plan sets short term goals for improved data collection on landings 
and discards, improved compliance and monitoring by the IBAMA, 
supervision of elasmobranch landings to ensure fins are landed with 
carcasses, the creation of a national port sampler program, and 
intensified on-board observer monitoring programs. Mid-term goals 
include increased monitoring and enforcement within protected areas as 
well as the creation of new protected areas based on essential fish 
habitat for the 12 species of concern. It also calls for improved 
monitoring of fishing from beaches in coastal and estuarine

[[Page 76073]]

environments. Long term goals call for improved ecological data and 
stock assessments for key species as well as mapping of elasmobranch 
spatiotemporal distributions. This data will be used to better inform 
the creation of protected areas and seasonal fishing closures. However, 
as stated above, the plan was only just approved as of December 2014, 
and will not be fully implemented for another 5 years. Even if the 
recommendations outlined in the plan are implemented in the future, it 
remains uncertain if they will be effective as the best available 
information suggests that current regulatory measures in Brazil to 
protect vulnerable species are poorly enforced, particularly within 
artisanal fisheries.
    Outside of Brazil, there is limited information on shark fishing 
regulations or their adequacy for protecting daggernose sharks from 
overutilization. In Guyana and Trinidad and Tobago, gillnet fisheries 
are restricted to using nets of 900 ft or less with no more than a 15-
foot depth; however, currently, there are no minimum size restrictions 
or catch quotas for sharks in either country (Shing 1999). As mentioned 
previously, both countries have open access fisheries (however, in 
Guyana the open access fishery only applies to the artisanal gillnet 
fishery) (FAO 2005a, 2006). In the late 1990s a fisheries management 
plan was drafted for Trinidad and Tobago, which prohibited the use of 
monofilament gillnets less than 4.75'' stretch mesh and developed a 
licensing system (Shing 1999); however, no further details about the 
plan, including effectiveness or enforcement of these regulations, 
could be found. According to Casselberry and Carlson (2015a), in the 
summer of 2013, Guyana's Fisheries Department within the Ministry of 
Agriculture passed a 5-year Fisheries Management Plan for Guyana to run 
from 2013 to 2018, with one aspect of this plan meant to address shark 
fishing, but no further details could be found at this time. 
Enforcement of existing fishery regulations is also lacking due to 
insufficient resources, with minimal control over the fisheries 
resulting in increasing competition and conflicts among fishermen and 
between fishing fleets and, consequently, overfishing of marine 
resources (FAO 2005a, 2005b, 2006, 2008). No other pertinent 
information could be found on shark fishing regulations or their 
adequacy in controlling the exploitation of sharks, and more 
specifically daggernose sharks.

Extinction Risk

    Although accurate and precise population abundance and trend data 
for the daggernose shark are lacking, best available information 
provides multiple lines of evidence indicating that this species 
currently faces a high risk of extinction. Below, we present the 
demographic risk analysis, threats assessment, and overall risk of 
extinction for the daggernose shark.

Demographic Risk Analysis

Abundance
    There is a significant lack of abundance information for I. 
oxyrhynchus throughout its range. In northern Brazil, the relatively 
recent (2004-2009) absence of the species in fish markets where they 
were once abundantly sold, in addition to their absence in fishery-
independent research surveys in areas where they were commonly caught 
prior to 1992, suggests the species has suffered significant declines 
in population abundance. Based on the daggernose shark's life history 
parameters and rates of fishing mortality, the population abundance in 
northern Brazil is estimated to have declined by 18.4 percent per year 
from the mid-1990s to mid-2000, resulting in a total population decline 
of at least 90 percent in approximately half of the species' known 
range. Although abundance information from the other parts of the 
species' range, including off Venezuela, Trinidad, Guyana, Suriname and 
French Guiana, is presently unavailable, it is thought that these 
populations have suffered similar declines based on the species' 
biological vulnerability and susceptibility to artisanal fisheries 
operating in these areas. Given the continued artisanal fishing 
pressure throughout the species' range, coupled with the species' 
present rarity and its potential extirpation in areas where it was 
previously abundant, it is likely that the species is still in decline, 
with current abundance trends and levels contributing significantly to 
its risk of extinction.
Growth Rate/Productivity
    The daggernose shark has extremely low productivity. Litter sizes 
range from 2-8 pups, with a 1-year gestation period and a year of 
resting between pregnancies. In other words, annual fecundity averages 
only 1-4 pups because of the species' biennial reproductive 
periodicity. Using these life history parameters, Casselberry and 
Carlson (2015a) estimated a productivity (as the intrinsic rate of 
population increase) of r = 0.004 year-\1\ (median) within a 
range of -0.040-0.038 (Carlson unpublished). Under natural mortality 
rates, Lessa et al. (2010) estimated annual population growth to be 
negative, with an r = -0.048 and a generation time of 9 years. When 
fishing mortality was considered, the estimate of r decreased even 
further, to -0.074, with a generation time of 8.4 years. Considering 
the daggernose shark has already undergone substantial population 
declines, and is still susceptible to fishing mortality in the active 
artisanal fisheries throughout its range, the species' extremely low 
productivity (with estimates of negative annual population growth 
rates) is likely significantly contributing to its risk of extinction.
Spatial Structure/Connectivity
    Very limited information is available regarding spatial structure 
and connectivity of the daggernose shark populations. The best 
available information suggests the daggernose shark has a very 
restricted range, one of the smallest of any elasmobranch species, and, 
as such, an increased vulnerability to extinction from environmental or 
anthropogenic perturbations. In addition, the substantial declines in 
the Brazilian population and subsequent absence of the species in areas 
it was previously known to occur, as well as its rarity throughout the 
rest of its range, suggest the species likely exists as patchy and 
small populations, which may limit connectivity. However, there is not 
enough information to identify critically important populations to the 
taxon as a whole, or determine whether the rates of dispersal among 
populations, metapopulations, or habitat patches are presently posing a 
risk of extinction.
Diversity
    The loss of diversity can increase a species' extinction risk 
through decreasing a species' capability of responding to episodic or 
changing environmental conditions. This can occur through a significant 
change or loss of variation in life history characteristics (such as 
reproductive fitness and fecundity), morphology, behavior, or other 
genetic characteristics. Although it is unknown if I. oxyrhynchus has 
experienced a loss of diversity, the significant decline estimated for 
the population in northern Brazil (comprising approximately half of its 
known range), as well as the likely small populations elsewhere 
throughout its range, suggest the species may be at an increased risk 
of random genetic drift and could experience the fixing of

[[Page 76074]]

recessive detrimental genes, reducing the overall fitness of the 
species.

Threats Assessment

    The primary threat to the daggernose shark is overutilization in 
artisanal fisheries. In Brazil, the species is bycaught in the 
artisanal gillnet fisheries for Spanish mackerel and king weakfish. 
Historically, the species comprised up to around 70 percent of the 
artisanal catch during the Amazonian summer in the State of 
Par[aacute], and was caught in large numbers by the artisanal gillnet 
fisheries operating on the Maranh[atilde]o coast in Brazil. However, 
given the extremely low productivity of the species and vulnerability 
to depletion, this level of exploitation resulted in substantial 
declines (estimated at over 90 percent) to the point where the species 
is no longer found in fish markets or observed in trawl and research 
survey data. The artisanal gillnet fisheries that were responsible for 
this decline are still active throughout the species' range and likely 
exerting similar fishing pressure that historically resulted in the 
substantial decline of the daggernose shark populations. In fact, 
together, the artisanal landings from the North region of Brazil (which 
includes the States of Amap[aacute] and Par[aacute]) and Northwest 
region (which includes the States of Maranh[atilde]o south to Bahia), 
the areas where daggernose sharks were once historically abundant, 
represent over 80 percent of the total artisanal landings for the 
entire country, indicating the importance and, hence, likely 
continuation of this type of fishing in these regions. Notably, the 
king weakfish fishery, which was reported as one of the two main 
artisanal gillnet fisheries responsible for bycatching daggernose 
sharks, remains one of the most important fisheries in Brazil.
    Artisanal gillnet fisheries are also active in the other parts of 
the species' range, including Venezuela, Trinidad and Tobago, Guyana, 
Suriname, and French Guiana, with likely similar fishing practices. 
Although landings data from these countries are unknown, the available 
information suggests that artisanal fishing pressure is high and that 
the species has been taken in small numbers by local fishermen in these 
countries, with daggernose sharks historically sold in markets in 
Trinidad and likely Guyana. Given the species' susceptibility to 
depletion from even low levels of fishing mortality, it is highly 
likely that overutilization by artisanal fisheries operating throughout 
the species' range is a threat that is significantly contributing to 
its risk of extinction.
    In 2004, the daggernose shark was listed on Brazil's endangered 
species list, and as of 2014, was classified as ``critically 
endangered.'' Additionally, it is listed as one of 12 species of 
concern under Brazil's FAO NPOA-sharks. However, the implementation and 
effectiveness of the recommendations outlined in this plan remain 
uncertain, with the best available information indicating that current 
regulatory measures in Brazil to protect vulnerable species are poorly 
enforced, particularly in artisanal fisheries (the fishery sector that 
poses the biggest threat of overutilization of the species). In 
addition, there appears to be a lack of adequate fishing regulations to 
control the exploitation of the daggernose shark in the other parts of 
its range, and, as such, the inadequacy of existing regulatory measures 
is a threat that further contributes to the extinction risk of the 
species.

Risk of Extinction

    Although there is significant uncertainty regarding the current 
abundance of the species, the species' population growth rate and 
productivity estimates indicate that the species has likely suffered 
significant population declines (of up to 90 percent) throughout its 
range and will continue to decrease without adequate protection from 
overutilization. The species' restricted coastal range, combined with 
its recent (2004-2009) absence in areas where it was once commonly 
found, as well as its present rarity throughout the rest of its range 
(with the last record of the species from 1999) indicate potential 
local extirpations and suggest an increased likelihood that the species 
is strongly influenced by stochastic or depensatory processes. This 
vulnerability is further exacerbated by the present threats of 
overutilization and inadequacy of existing regulatory measures that 
will significantly contribute to the decline of the existing 
populations (based on its demographic risks) into the future, 
compromising the species' long-term viability. Therefore, based on the 
best available information and the above analysis, we conclude that I. 
oxyrhynchus is presently at a high risk of extinction throughout its 
range.

Protective Efforts

    With the exception of the recommendations within Brazil's FAO NPOA-
sharks (discussed above), we were unable to find any other information 
on protective efforts for the conservation of daggernose sharks in 
Brazil, Venezuela, Trinidad and Tobago, Guyana, Suriname, or French 
Guiana that would potentially alter the extinction risk for the 
species. We seek additional information on other conservation efforts 
in our public comment process (see below).

Proposed Determination

    Based on the best available scientific and commercial information 
as presented in the status review report and this finding, we find that 
the daggernose shark is presently in danger of extinction throughout 
its range. We assessed the ESA section 4(a)(1) factors and conclude 
that that the species faces ongoing threats from overutilization and 
inadequacy of existing regulatory mechanisms throughout its range. The 
species' natural biological vulnerability to overexploitation and 
present demographic risks (e.g., low and declining abundance, negative 
population growth rates, small, fragmented and likely isolated 
populations, extremely restricted distribution, and very low 
productivity) are currently exacerbating the negative effects of the 
aforementioned threats, placing this species in danger of extinction. 
We also found no evidence of protective efforts for the conservation of 
daggernose shark that would reduce the level of extinction risk faced 
by the species. We therefore propose to list the daggernose shark as an 
endangered species.

Brazilian Guitarfish (Rhinobatos horkelii)

Species Description

    The Brazilian guitarfish (Rhinobatos horkelii) is a member of the 
order Rajiformes and the family Rhinobatidae (Lessa and Vooren 2007). 
The species within the family Rhinobatidae are very similar 
morphologically, which can make them difficult to distinguish from each 
other (De-Franco et al. 2010). The Brazilian guitarfish has long 
nostrils with transversely flat or a slightly convex crown and has a 
median row of tubercles (nodules) on its dorsal surface that are large 
and thorn-like (Lessa and Vooren 2005). The disc width is about 5/6 of 
the body length, with dorsal fins that are triangular and similar in 
size (Bigelow and Schroeder 1953). The dorsal side of the Brazilian 
guitarfish is olive grey or chocolate brown in color and lacks light or 
dark markings. Additionally, its snout has a ``sooty'' oval patch 
(Lessa and Vooren 2005).

Range and Habitat Use

    The Brazilian guitarfish is found along the coast of South America 
in the southwestern Atlantic from Bahia, Brazil to Mar del Plata, 
Argentina (Figueiredo 1977; Lessa and Vooren 2005, 2007; GBIF 2013). 
Newborns and

[[Page 76075]]

juveniles live year round in coastal waters less than 20 m deep. Adults 
coexist with immature individuals in shallow waters between November 
and March, when pupping and mating occur, but spend the rest of the 
year offshore in waters greater than 40 m depth. In the winter, 
individuals can be found in water temperatures as low as 9 [deg]C, 
while in the summer, individuals are found in average water 
temperatures of 26 [deg]C (Lessa and Vooren 2005). Brazilian guitarfish 
are commonly found in salinities ranging from 24-28 ppt in northern 
Argentina (Jaureguizar et al. 2006).

Diet and Feeding

    There is very little information on the diet or feeding behavior of 
Brazilian guitarfish. Refi (1973) recorded the stomach contents of six 
individuals caught in Mar del Plata, Argentina and found that stomachs 
contained the Patagonian octopus (Octopus tehuelchus), shrimp 
(Hymenopeneus muelleri), decapods, isopods, and polychaetes. No other 
information on diet or feeding could be found.

Growth and Reproduction

    Based on a yearly vertebral annulus formation in September, Vooren 
et al. (2005a; citing Lessa (1982)) report the von Bertalanffy growth 
rate (k) for Brazilian guitarfish to be 0.0194, with a theoretical 
maximum size of 135.5 cm TL and age at maturity between 7 and 9 years 
for females and 5 and 6 years for males. Similar results were estimated 
by Caltabellota (2014), with a theoretical maximum size of 121.71 cm TL 
and k = 0.21. No significant differences were found in growth between 
the sexes. Using two different methods, Caltabellota (2014) also 
estimated theoretical longevity of 18.24 and 14.17 years for females, 
and 13.86 and 10.90 years for males. Vooren et al. (2005a) found 
longevity to be longer for both females and males, with estimates of 28 
years and 15 years, respectively.
    Size at maturity for Brazilian guitarfish is between 90 cm and 120 
cm TL for both sexes; the smallest pregnant females recorded were 
between 91-92 cm TL, and all captured females larger than 119 cm TL 
were pregnant (Lessa et al. 2005a; Lessa and Vooren 2005). The 
Brazilian guitarfish has an annual reproductive cycle, with 
lecithotrophic development (i.e., larva depend on the egg's yolk 
reserve supplied by the mother), and a gestation period lasting 
approximately 11-12 months (Lessa et al. 2005a; Lessa and Vooren 2005). 
Gravid females live at depths greater than 20 m for most of the year, 
but migrate into the shallows in the spring and summer to give birth. 
Litter sizes range from 4-12 pups and increase with female size (Lessa 
and Vooren 2005).

Genetics and Population Structure

    Studies examining the genetics of the species or information on its 
population structure could not be found.

Demography

    Total natural mortality for Brazilian guitarfish was estimated by 
Caltabellota (2014) using an age at maturity of 5 years (i.e., an 
earlier age of maturity than what was reported by Vooren et al. 
(2005a)), and found the estimated total natural mortality from catch 
curves to be 0.692 for males and 0.751 for females. Modeling of various 
exploitation scenarios found that under natural conditions, with no 
fishing mortality, the population would increase by 9 percent each 
year, with a population doubling time of 7.41 years (Caltabellota 
2014). In the presence of fishing mortality and an age at first capture 
of 2 years, the Brazilian guitarfish population would decline by 25 
percent every 2.73 years; however, if the age at first capture was 
after the age at first maturity (assumed to be 5 years for these 
models), the population would increase by 4 percent each year 
(Catabellota 2014). Based on the life history parameters discussed 
previously, these demographic parameters indicate that the Brazilian 
guitarfish generally has a low potential to recover from exploitation, 
particularly if the species is experiencing fishing pressure on 
neonates and juveniles.

Historical and Current Distribution and Population Abundance

    The Brazilian guitarfish is distributed along the coast of South 
America, from Bahia, Brazil to Mar del Plata, Argentina. The species' 
center of distribution lies between 28[deg] and 34[deg] S. and also 
corresponds to the area where it is most abundant. This area is known 
as the Plataforma Sul, which includes the continental shelf of southern 
Brazil and extends from Cabo de Santa Marta Grande (28[deg]36' S.) to 
Arroio Chu[iacute] (33[deg]45' S.). In historical bottom trawl surveys 
between latitudes 28[deg]00' S. and 34[deg]30' S., R. horkelii was 
common across the Plataforma Sul south of latitude 29[deg]40' S. 
(Vooren et al. 2005a). Annual catch of Brazilian guitarfish in this 
area was approximately 636 t-1803 t from 1975-1987 (Miranda and Vooren 
2003). Research surveys conducted between Chu[iacute] and 
Solid[atilde]o (Rio Grande do Sul, Brazil) in February 2005 found an 
average CPUE of 1.68 kg/hr (Vooren et al. 2005b), but no follow-up 
surveys were conducted after 2005.
    Throughout the rest of its range, there is little information on 
the abundance of R. horkelli, with the species considered to be a rare 
occurrance. In northern Argentina (34[deg] S.-43[deg] S.), estimated 
mean biomass of Brazilian guitarfish was 0.1240 t/nm\2\ between 1981 
and 1999, with R. horkelli comprising only 0.44 percent of the biomass 
of demersal fish on the northern Argentine continental shelf 
(Jaureguizar et al. 2006). In 1981, biomass of Brazilian guitarfish was 
calculated to be 0.010 t/nm\2\ in 1981. Estimated biomass then peaked 
at 0.441 t/nm\2\ in 1994 before falling steadily to 0.007 t/nm\2\ in 
1999 (Jaureguizar et al. 2006). Biomass estimates reported in 
Argentina's FAO NPOA-sharks for the coast of Buenos Aires province and 
Uruguay were 2,597 t in 1994, 661 t in 1998, and 91 t in 1999 
(Argentina FAO NPOA-sharks 2009). Along the oceanic coast of Uruguay, 
R. horkelii occurs with low density, with annual catches around 3 t in 
2000 and 2001 (Meneses 1999; Paesch and Sunday 2003).

Summary of Factors Affecting the Brazilian Guitarfish (Rhinobatos 
horkelii)

    We reviewed the best available information regarding historical, 
current, and potential threats to the Brazilian guitarfish species. We 
find that the main threat to this species is overutilization for 
commercial purposes. We consider the severity of this threat to be 
exacerbated by the species' natural biological vulnerability to 
overexploitation, which has led to significant declines in abundance of 
all life stages, particularly neonates. We find current regulatory 
measures inadequate to protect the species from further 
overutilization. Hence, we identify these factors as additional threats 
contributing to the species' risk of extinction. We summarize 
information regarding these threats and their interactions below 
according to the factors specified in section 4(a)(1) of the ESA. 
Available information does not indicate that habitat destruction or 
curtailment, disease, predation or other natural or manmade factors are 
operative threats on these species; therefore, we do not discuss these 
factors further in this finding. See Casselbury and Carlson (2015b) for 
discussion of these ESA section 4(a)(1) threat categories.

[[Page 76076]]

Overutilization for Commercial, Recreational, Scientific, or 
Educational Purposes

    Based on historical catch data and trends, the primary threat to 
Brazilian guitarfish is overutilization in industrial and artisanal 
fisheries. Before landings were prohibited in Brazil in 2004, the 
Brazilian guitarfish was considered to be the only economically 
important species of the order Rajiformes in southern Brazil, where 
they were fished and caught in otter trawls, pair trawls, shrimp 
trawls, beach seines, and bottom gillnets (Haimovici 1997; Mazzoleni 
and Schwingel 1999; Martins and Schwingel 2003; Lessa and Vooren 2005). 
Commercial catches of the Brazilian guitarfish primarily occurred 
between 28[deg] S.-34[deg] S. in Brazil, where the species is most 
heavily concentrated (Martins and Schwingel 2003; Lessa and Vooren 
2005). The pair and simple trawl fleets, which operate on the inner 
continental shelf and outer shelf, respectively, were responsible for 
the majority of the commercial R. horkelli catch in the 1970s and 1980s 
(Vooren et al. 2005a). Based on historical data, CPUE for the pair 
trawling fleet was highest from December to March, when adults of the 
species would concentrate in coastal waters during the summer for 
birthing and reproduction purposes (making them, as well as their 
young, more susceptible to being caught in large numbers by the 
trawlers) (Miranda and Vooren 2003; Vooren et al. 2005a). In the winter 
(April to September), the simple trawl fleet saw an increase in CPUE as 
both juvenile and adult Brazilian guitarfish migrated to the outer 
shelf; however, as the species was able to spread out more on the outer 
shelf, the CPUE of the simple trawl fleet tended to be half of what the 
pair trawling fleet experienced (Miranda and Vooren 2003; Vooren et al. 
2005a). Regardless, given the effort and complementary spatial and 
temporal operations of these fleets, the adult population of Brazilian 
guitarfish was under high fishing pressure year-round. Consequently, 
this level of exploitation led to significant decreases in the 
abundance of the species, as evidenced by the substantial declines in 
landings and CPUE from both of these fleets. From 1975 to 1986, 
Brazilian guitarfish were common in the landings of these two fleets 
that were operating from Rio Grande do Sul, averaging more than 100 t 
annually in the simple trawl fleet and more than 200 t annually in the 
pair trawl fleet (Klippel et al. 2005). The simple trawl fleet saw 
maximum landings of Brazilian guitarfish in the years 1976 (228 t) and 
1984 (219 t) and the pair trawl fleet landed a Brazilian industrial 
fishing record amount of 1,014 t of R. horkelli in 1984 (Klippel et al. 
2005). However, both fleets saw a significant drop in landings and CPUE 
after 1986. After 1987, landings oscillated between 50 t and 200 t 
annually for the pair trawl fleet, and from 1991-2000, annual landings 
did not exceed 10 t for the single trawl fleet (Klippel et al. 2005). 
In terms of CPUE, the simple trawl fleet saw an 84 percent decline 
between 1975-1986 and 1993-1999, with CPUE decreasing from 0.55 t/trip 
(range: 0.41-0.94) to 0.09 t/trip (range: 0.04-0.15) for the respective 
time periods (Vooren et al. 2005a). Similarly, the pair trawl fleet 
CPUE decreased from 1.07 t/trip (range: 0.43-2.38) to 0.18 t/trip 
(range: 0.09-0.30), an 83 percent decline between the two time periods 
(Vooren et al. 2005a). Based on these landings and CPUE data, the 
Brazilian guitarfish population on the Plataforma Sul is thought to 
have collapsed after 1986, with the abundance of the species after 1993 
estimated to be around 16 percent of its 1986 level (Vooren et al. 
2005a).
    From 2000 to 2002, increases in CPUE of R. horkelli were recorded 
off Santa Catarina, Brazil, in both pair trawls (from 0.11 t/trip in 
2000 to 0.15 t/trip in 2002) and single trawls (from 0.63 t/trip in 
2001 to 1.0 t/trip in 2002) (Martins and Schwingel 2003). However, 
these increases were assumed to be a reflection of changes in 
operational fishing strategy as opposed to an increase in guitarfish 
abundance (Martins and Schwingel 2003). In 2000, the single and pair 
trawl fleets operating out of Itajai (Santa Catarina, Brazil) began 
fishing in depths of 100 m-200 m on the outer continental shelf and 
slope between 28[deg] S.-30[deg] S., which was previously unexplored 
fishing grounds by these trawl fleets (Martins and Schwingel 2003; 
Vooren et al. 2005a). These fleets subsequently caught large amounts of 
Brazilian guitarfish in the autumn and winter, of which the majority 
were juveniles (Vooren et al. 2005a; Klippel et al. 2005). In fact, 
based on a sample of landings data between 2002 and 2003, juveniles 
(<90 cm) comprised around 81 to 94 percent of the R. horkelli catch 
from the industrial trawl fleets, and 76 percent in the bottom gillnet 
fleet (Klippel et al. 2005). This increase in R. horkelli catch by the 
industrial fleets was attributed to their fishing in a previously 
unexplored outer shelf and slope habitat that likely constituted a 
haven for part of the Plataforma Sul population of Brazilian guitarfish 
(Martins and Schwingel 2003). Although it was determined that these 
fleets were not specifically targeting R. horkelli (based on the fact 
that the species comprised only around 1-2.5 percent of the total catch 
in 2002 and 2003), decreases in the CPUE of R. horkelli between 2002 
and 2003 suggest that the population was already being impacted by the 
increase in fishing pressure in this area (Vooren et al. 2005a). 
Specifically, the R. horkelli CPUE of these fleets declined from 663 
kg/trip in 2002 to 456 kg/trip in 2003 (Vooren et al. 2005a), which 
equates to a decline of 31 percent and is concerning for a population 
that has already been fished to such low levels. In fact, in July 2010, 
the state of S[atilde]o Paulo, Brazil declared the stock of Brazilian 
guitarfish collapsed due to intense exploitation, with biomass and the 
stock's reproductive potential at such a level that severely comprises 
recovery.
    In addition to the contribution of the industrial fisheries to the 
overutilization of the species, artisanal fisheries were also known for 
catching large quantities of the Brazilian guitarfish in beach seines 
and fixed nets (Miranda and Vooren 2003; Lessa and Vooren 2005). In 
fact, before the prohibition of the species, artisanal fisheries, 
combined with the industrial pair trawl fisheries, caught over 70 
percent of the Brazilian guitarfish (Miranda and Vooren 2003). Because 
these artisanal fisheries operate on the inshore pupping grounds of the 
species, the guitarfish catch consists primarily of aggregations of 
pregnant females (around 98 percent of the catch) (Lessa and Vooren 
2005). In the 1980s, annual artisanal catches of guitarfish wavered 
around 600 t-800 t but declined soon after (Lessa, 1982; Miranda and 
Vooren 2003). In 1992, artisanal landings were estimated at 330 t and 
by 1997, landings dropped to only 125 t, a decrease that was attributed 
to a reduction in catches specifically of R. horkelli (Miranda and 
Vooren 2003). Monitoring of 20 artisanal beach seine fishing operations 
in 2002/2003 documented only a single haul containing R. horkelli, and 
artisanal fishermen now report that catches of Brazilian guitarfish are 
rare (Vooren et al. 2005a). Due to this significant decline in 
abundance of the species, artisanal fishermen have shifted their focus 
to fishing for mullet (Vooren et al. 2005a). However, they still 
operate within the R. horkelli inshore pupping grounds on the 
Plataforma Sul, and, as such, the species remains susceptible to 
incidental capture in beach seines and fixed net fishing gear (Vooren 
et al. 2005a). Recent data also indicate that when Brazilian guitarfish 
are caught by

[[Page 76077]]

artisanal fishermen, the species is not usually released, despite its 
prohibited status (Vooren et al. 2005a; Vieira 2014). For example, from 
November 2013 to March 2014, Vieira (2014) monitored four artisanal 
fishing boat operations (off Rio Grande do Sul) that made 50 sets over 
20 fishing trips in depths of 5 m to 21 m using primarily gillnets. The 
Brazilian guitarfish was the second most abundant species caught by 
gillnets, with 125 individuals captured, representing 17.5 percent of 
elasmobranch catch. Its frequency of occurrence per fishing trip was 40 
percent. The author noted that all of the caught sharks (either as 
catch or bycatch) were sold, whereas out of all the caught rays, only 
R. horkelli was sold. Additionally, although the CPUE was estimated to 
be relatively low for the elasmobranchs in the study, given the area 
where these artisanal fisheries operate, the majority of the R. hokelli 
catch consisted of immature individuals and breeding adults (with 
observations of pregnant females initiating abortion on the boats) 
which likely compromises recruitment to the already at risk population 
(Vieira 2014).
    The substantial abundance declines of R. horkelli on the Plataforma 
Sul due to overutilization by fisheries, as indicated by the commercial 
and artisanal fisheries data, is further confirmed by CPUE data from 
fishery-independent surveys of the region. On the Plataforma Sul, a 
number of research cruises dating back to 1972 have surveyed the area 
using bottom trawl gear (from depths of around 10 m to over 500 m). In 
an analysis of this time series set, Vooren et al. (2005a) note that 
between the periods of 1975-1986 and 1993-1999, CPUE of R. horkelli 
showed similar declines as those observed in the commercial CPUE over 
the same period. Based on the CPUE trends, abundance of R. horkelli on 
the Plataforma Sul in depths of 20 m-200 m is estimated to have 
decreased by about 85 percent between 1975 and 1999 (Vooren et al. 
2005a).
    Overall, based on the above commercial and artisanal fishing data, 
it is estimated that over the period of 1975-1986, around 100,000 
mature R. horkelli females and 100,000 mature R. horkelli males were 
caught annually (Vooren et al. 2005a). The removal of these 
reproductively active adults from the population translated to a loss 
of around 600,000 newborns per year, or 6.7 million newborns over the 
course of the 11-year period of fishing, and led to recruitment 
overfishing of the species (Vooren et al. 2005a). As a result of this 
overutilization, abundance of the species on the Plataforma Sul 
significantly declined, causing the stock to collapse after 1986.
    Overutilization still remains a threat to the species as fishing by 
the industrial and artisanal fleets continues to occur at high efforts 
on the Plataforma Sul and especially within important nursery habitats 
for the species (Vooren et al. 2005a; Klippel et al. 2005; Vooren and 
Klippel 2005c). In 2007, the industrial fleets operating off southern 
Brazil, where R. horkelli is most concentrated, and specifically from 
the States of Parana, Santa Catarina, and Rio Grande du Sol (identified 
as Brazil's ``South Region''), were responsible for landing around 54 
percent (151,154 mt) of the total industrial fish catch for all of 
Brazil (277,364.5 mt). Within Brazil's South Region, the industrial 
fleet comprised 59.3 percent of the total fish landings from the region 
(255,080.5 mt). In 2011, the South Region's marine fish landings (not 
including aquaculture) amounted to 158,515.4 mt, representing 47 
percent of the total fish production from that region and 28.6 percent 
of the national total of marine fish landings. In terms of artisanal 
fisheries, fishing pressure (and related mortality) on R. horkelli is 
likely high given that the mullet fishery, the target of artisanal 
fisheries operating within R. horkelli nursery habitats, is an 
important fishery in Brazil. According to Lemos et al. (2014), catches 
of mullets (Mugil liza) in Rio Grande do Sul and Santa Catarina between 
1997 and 2010 were around 95 percent of the total catch from all other 
Brazilian states, Uruguay, and Argentina. In 2011, mullets were the 2nd 
most landed fish (in terms of volume) in the artisanal fisheries in Rio 
Grande do Sul (IBAMA/Centro de Pesquisa e Gest[atilde]o dos Recursos 
Pesqueiros Lagunares e Estuarinos (CEPERG) 2012) and the 5th most 
landed marine fish species for all of Brazil, with landings totaling 
18,045 t (MPA 2011), suggesting that this significant fishing effort by 
artisanal fisheries in the inshore pupping grounds of Brazilian 
guitarfish is unlikely to decrease in the foreseeable future. 
Additionally, the relatively recent expansion and operation of the Rio 
Grande do Sul and Itajai trawl fleets on the outer shelf and continued 
operation of the pair trawl fleet on the inner continental shelf 
suggest overutilization (in the form of bycatch mortality) is still a 
threat to the species. Areas that previously served as offshore refugia 
for the Plataforma Sul population from fishing pressure are no longer 
protected from exploitation, with both juveniles and adults susceptible 
to fishery-related mortality over their entire habitat.

Inadequacy of Existing Regulatory Mechanisms

    Like the daggernose shark, the Brazilian guitarfish was also listed 
on Brazil's endangered species list in 2004, and as of 2014, was 
classified as ``critically endangered.'' In 2007, Lessa and Vooren 
noted that the 2004 prohibition on catching the species was gradually 
becoming more effectively enforced, but genetic studies indicate that 
enforcement was still relatively poor as recently as 2009. Of 267 
guitarfish samples that were collected at ports throughout southeastern 
and southern Brazil between 2008 and 2009, 55.8 percent were 
genetically identified as Brazilian guitarfish (De-Franco et al. 2012). 
Of the 85 samples from boats operating off Santa Catarina, 100 percent 
of the guitarfish were Brazilian guitarfish (De-Franco et al. 2012). 
When the fishermen were asked about their landings during sample 
collection, many of them denied harvest of guitarfish, suggesting that 
fishermen are aware of the capture prohibition of Brazilian guitarfish 
(De-Franco et al. 2012). However, because fishermen commonly remove the 
head and gut of any guitarfish before arriving in port, distinguishing 
the Brazilian guitarfish from the other two guitarfish species in the 
area (R. percellens and Zapteryx brevirostris) is difficult, which, 
when coupled with the lack of adequate government inspections, may be 
encouraging fishermen to disregard the law for economic gain (De-Franco 
et al. 2012). Similarly, and most recently, a 2013 investigation by Sea 
Shepherd Brazil into the illegal trade of elasmobranchs by the 
S[atilde]o Paulo General Warehousing and Centers Company led to the 
seizure of 700 kg of illegal elasmobranch species by federal police. 
Included in the illegal haul were Brazilian guitarfish, again 
suggesting that poor enforcement of present regulations is likely 
contributing to the continued exploitation and, consequently, 
overutilization of the species.
    Although the Brazilian guitarfish occurs in several MPAs within 
Brazilian waters, including APA de Canan[eacute]ia-Iguape-
Peru[iacute]be (S[atilde]o Paulo; 234,000 hectares), PARNA do Superagui 
(Parana; 33,988 hectares), REBIO do Arvoredo (Santa Catarina; 17,600 
hectares) and RESEX Marinha do Pirjuba[eacute] (Santa Catarina; 1,712 
hectares) (Rosa and Lima 2005), these MPAs only protect the species 
from exploitation when they occur within these areas. In addition, the 
coverage of these MPAs compared to

[[Page 76078]]

the range of the species is very small and also located north of the 
center of distribution and concentration of the species and, therefore, 
unlikely to significantly decrease the threat of overutilization to the 
species.
    Another regulation in place in Brazil to control the exploitation 
of marine resources is a prohibition on trawl fishing within three 
nautical miles (nm) from the coast of southern Brazil. This prohibition 
may help decrease fishery-related mortality of R. horkelli in the 
nearshore areas primarily used as nursery habitat by the species; 
however, according to Chiaramonte and Vooren (2007), enforcement of 
this prohibition has been noted as difficult. In addition, the species 
is still susceptible to being caught as bycatch in the legally 
permitted coastal gillnet fisheries (which also operate in nursery 
areas) and in the offshore trawl and gillnet fisheries and vulnerable 
to the associated bycatch mortality (Lessa and Vooren 2007). Therefore, 
the adequacy of the trawl prohibition in decreasing fishery-related 
mortality of R. horkelli to the point where the extinction risk of the 
species is significantly lowered is unclear.
    Like the daggernose shark, the Brazilian guitarfish is one of 
Brazil's 12 species of concern identified in their FAO NPOA-sharks. The 
plan recommends a moratorium on fishing with a prohibition of sales 
until there is scientific evidence in support of recovery, and proposes 
a fishing exclusion area over a large region of the coast of Rio Grande 
do Sul at depths of 20 m to protect nursery areas (No 125, Lessa et al. 
2005). As noted in the daggernose shark analysis above, this plan will 
not be fully implemented for another 5 years and it remains uncertain 
whether the recommendations will be implemented and effective, as the 
best available information suggests that current regulatory measures in 
Brazil to protect the Brazilian guitarfish are poorly enforced.
    Similar to Brazil, Uruguay also lists the Brazilian guitarfish as a 
species of high priority in its FAO NPOA-sharks (Domingo et al. 2008). 
The plan sets short-term goals (12-18 months) to investigate 
distribution and habitat use and generate time-series of effort and 
catch; mid-term goals (24-30 months) to conduct an abundance assessment 
and determine maximum sustainable catch limits; and long term goals 
(36-48 months) to conduct age, growth, reproduction, and diet studies. 
In its plan, Uruguay made it a priority to: Review current fishing 
licenses that allow for the catch of Brazilian guitarfish and possibly 
modify them; no longer grant new licenses that would allow for such 
fishing; forbid processing and marketing of the species; and promote 
safe release if possible. However, updated results from the goals and 
priorities of this plan could not be found. As such, their 
implementation and overall effectiveness at decreasing the threats to 
the species remains highly uncertain.

Extinction Risk

    The best available information provides multiple lines of evidence 
indicating that the R. horkelli currently faces a high risk of 
extinction. Below, we present the demographic risk analysis, threats 
assessment, and overall risk of extinction for the Brazilian 
guitarfish.

Demographic Risk Analysis

Abundance
    There is very limited information regarding abundance estimates for 
R. horkelli throughout its range. The majority of the Brazilian 
guitarfish population and center of distribution is concentrated 
between 28[deg] S. and 34[deg] S. in southern Brazil, and it is scarce 
elsewhere. On the northern Argentine continental shelf, between 34[deg] 
S. and 43[deg] S., which appears to be the southern extent of the 
species' range, mean biomass of R. horkelli has fluctuated over the 
years. In 1981, biomass was estimated to be 0.010 t/nm\2\. Biomass 
peaked in 1994 at 0.441 t/nm\2\ before falling to 0.007 t/nm\2\ in 1999 
(Jaureguizar et al. 2006). This represents a 98 percent decrease from 
peak biomass between 1994-1999, but only a decrease of around 30 
percent from estimates in 1981. While mean abundance estimates from the 
presumed center of the species' distribution are not available, we can 
infer significant historical population declines from a variety of 
fishery effort, catch and landings data from this region. Based on both 
fishery-independent sampling and commercial fleet CPUE data from 1975-
1986 and 1993-2002, the population of Brazilian guitarfish along the 
southern coast of Brazil has significantly decreased in size. Data from 
the single and pair trawl fleets operating on the Plataforma Sul 
indicate that CPUE declined by 61 percent and 74 percent, respectively, 
between the periods of 1975-1986 and 1993-2002 (Klippel et al. 2005). 
The population is assumed to have collapsed after 1986. Since 1993, the 
population is estimated to be about 16 percent of its 1986 level. Due 
to species identification issues, there is some level of uncertainty 
regarding the accuracy of the available data; however, based on the 
best available information (including fisheries-independent survey 
data), it appears that the species has likely undergone significant 
declines throughout its range. Given the continued high fishing 
pressure in the species' nursery grounds and presence of the species in 
recent landings data despite its prohibited status, abundance has 
likely continued to decline.
Growth Rate/Productivity
    Lessa and Vooren (2005) estimated the growth rate of R. horkelii as 
(k) = 0.194, and more recently, Caltabellota (2014) reported similar 
results, with an estimated k = 0.21 (with no significant difference in 
growth rates between sexes). The species is thought to reproduce 
annually, with a long gestation period (~1 year) and low fecundity 
(litter sizes range from 4 to 12 pups). Females have also been observed 
aborting embryos upon capture in fishing gear, further decreasing the 
reproductive output of the species. In addition, based on the data, it 
appears that both males and females of the species do not reach 
reproductive maturity until they have grown to approximately 74-89 
percent of their maximum size. These reproductive characteristics 
suggest the species has relatively low productivity, similar to other 
elasmobranch species, which likely hinders its ability to quickly 
rebound from threats that decrease its abundance (such as 
overutilization).
    Under natural mortality, Caltabellota (2014) estimated that the 
population would increase by 9 percent each year, doubling every 7.41 
years. However, if individuals of the species are fished before 
reaching maturity (assumed to be 5 years), the Brazilian guitarfish 
population will decline by 25 percent every 2.73 years (Caltabellota 
2014). Given the historical declines in CPUE and levels of neonate and 
juvenile landings, the species was likely subject to this exploitation 
scenario and subsequently experienced a negative population growth rate 
to the point where the population collapsed after 1986. With the 
continued fishing pressure by the mullet fisheries operating in the 
nursery habitats and the industrial fisheries on the Plataforma Sul, 
the available data on growth rate and productivity of the species 
indicates that current exploitation levels will likely continue to 
cause population declines in the species, with no information to 
suggest this trend is reversing.
Spatial Structure/Connectivity
    The species is thought to have a continuous distribution along the

[[Page 76079]]

Plataforma Sul (where the species is most abundant) (Vooren et al. 
2005a); however, there is no information on the connectivity among 
other R. horkelii populations throughout the rest of its range, 
including the importance of the Plataforma Sul population to the taxon 
as a whole. Based on the available data, there is not enough 
information to identify critical populations or determine whether the 
rates of dispersal among populations, metapopulations, or habitat 
patches are posing a risk of extinction to the species.
Diversity
    The loss of diversity can increase a species' extinction risk 
through decreasing a species' capability of responding to episodic or 
changing environmental conditions. This can occur through a significant 
change or loss of variation in life history characteristics (such as 
reproductive fitness and fecundity), morphology, behavior, or other 
genetic characteristics. Although it is unknown if R. horkelli has 
experienced a loss of diversity, the significant reduction in 
population size on the Plataforma Sul, as well as the likely small 
populations elsewhere throughout its range, suggest the species may be 
at an increased risk of random genetic drift and could experience the 
fixing of recessive detrimental genes, reducing the overall fitness of 
the species.

Threats Assessment

    Present threats to the species include overutilization by fisheries 
and inadequate regulatory mechanisms. The artisanal and industrial 
fisheries that historically contributed to the decline in R. horkelii 
are still active throughout the species' range and significantly 
contribute to national marine fish production. In fact, in Brazil in 
2007, the industrial fleets were responsible for landing over half of 
the marine fish from the country's South Region, where R. horkelli is 
most concentrated, with artisanal fisheries responsible for 10 percent. 
The most recent statistics from 2011 show that marine fish landings 
from the South Region represent almost half of the fish production from 
that region and 28.6 percent of the Brazilian national total of marine 
fish landings. Because these artisanal and industrial fleets primarily 
operate in locations where R. horkelii would occur, and use rather 
unselective fishing gear, their operations are likely contributing 
significantly to the fishery-related mortality rates of the species and 
impacting the status of the species.
    Although trawl fishing in Brazil is prohibited within 3 nm of the 
coast (<10 m depth), the shallow nursery areas, where neonates are 
found year-round and where adults are concentrated during the pupping 
and mating season, are still accessible to and heavily fished by 
artisanal fisheries using gillnets and beach seines. For example, in 
the mullet fishery, fishermen use beach seines to trap the mullets; 
however, due to the low selectivity of the fishing gear, these seines 
may also catch large numbers of juvenile and pregnant female guitarfish 
as evidenced by the historical data from beach seine operations on the 
coast of Rio Grande do Sul (Miranda and Vooren 2003; Lessa and Vooren 
2005; Vooren et al. 2005a). The mullet fishery remains an important 
fishery in Brazil and in 2011, mullets were the 2nd most landed fish in 
the Rio Grande do Sul artisanal fisheries and the 5th most landed 
marine fish in all of Brazil. Additionally, the artisanal gillnet 
fisheries operating off Rio Grande do Sul are also known to bycatch and 
sell pregnant females, mature males, and juvenile Brazilian guitarfish, 
despite its prohibited status. Based on the modeled exploitation 
scenarios and resultant population growth rates described in the 
demographic analysis above, continued fishing pressure by both 
artisanal fisheries targeting mullet, as well as other gillnet 
fisheries, and subsequent fishery-related mortality of immature 
Brazilian guitarfish, is likely contributing to the significant decline 
of the species and is a threat that places the species at a high risk 
of extinction.
    In addition to the threat from artisanal fishing operations, 
juveniles and adults of the species are also at risk of bycatch-related 
mortality by the industrial trawl and gillnet fleets operating off Rio 
Grande do Sul and Santa Catarina. These fleets focus trawling efforts 
on the inner and outer continental shelf (between 29[deg] S. and 
34[deg] S.), essentially covering the entire seasonal adult migratory 
corridor. Of concern is the fact that the R. horkelli catch from these 
industrial fleets are predominantly juveniles, with estimates of 
juveniles comprising around 76 to 94 percent of the landings from these 
fleets. Again, based on the modeled exploitation scenarios, this level 
of juvenile catch is likely contributing to significant declines in the 
population. Additionally, the relatively recent expansion and operation 
of the Rio Grande do Sul and Itajai trawl fleets into previously 
unexplored depths of 100 m-200 m on the outer shelf 28[deg] S.-30[deg] 
S., and the subsequent large catches of Brazilian guitarfish, also 
suggest that areas that previously served as offshore refugia for the 
Rio Grande do Sul population from fishing pressure are no longer 
protected from exploitation.
    In July 2010, the State of S[atilde]o Paulo, Brazil, declared the 
stock of Brazilian guitarfish collapsed due to intense exploitation. 
Despite the species' listing under Brazil's endangered species list 
since 2004, which effectively prohibits catching this species, R. 
horkelli continues to be brought into ports throughout southeastern and 
southern Brazil. In both Brazil and Uruguay, R. horkelli is considered 
a species of high priority under the country's respective FAO NPOA-
sharks. However, the implementation and effectiveness of the 
recommendations outlined in these plans remain uncertain, with the best 
available information indicating that current regulatory measures to 
protect vulnerable species are poorly enforced, particularly within 
artisanal fisheries. Overall, the best available information suggests 
heavy exploitation of R. horkelli, particularly in the area where it 
was historically most abundant, and a significant lack of adequate 
regulatory mechanisms to protect the species from overutilization 
throughout its range.

Risk of Extinction

    Although there is significant uncertainty regarding the current 
abundance of the species, the best available information indicates that 
the species has suffered significant historical population declines, 
with no indication that these trends have stabilized or reversed. Based 
on the species' demographic risks, without adequate protection, these 
severely depleted populations are likely to be strongly influenced by 
stochastic or depensatory processes. This vulnerability is further 
exacerbated by the present threats of overutilization and inadequacy of 
existing regulatory measures that continue to contribute to the decline 
of the existing populations, compromising the species' long-term 
viability. Therefore, based on the best available information and the 
above analysis, we conclude that the R. horkelli is presently at a high 
risk of extinction throughout its range.

Protective Efforts

    With the exception of the recommendations within Brazil and 
Uruguay's FAO NPOA-sharks plans discussed above, we were unable to find 
any other information on protective efforts for the conservation of 
Brazilian guitarfish in Brazil, Uruguay, or Argentina that would 
potentially alter the extinction risk for the species. We seek 
additional information on other conservation efforts in our public 
comment process (see below).

[[Page 76080]]

Proposed Determination

    Based on the best available scientific and commercial information 
as presented in the status review report and this finding, we find that 
the Brazilian guitarfish is presently in danger of extinction 
throughout its range. We assessed the ESA section 4(a)(1) factors and 
conclude that the species faces ongoing threats from overutilization 
and inadequacy of existing regulatory mechanisms throughout its range. 
The species' natural biological vulnerability to overexploitation and 
present demographic risks (e.g., low and declining abundance, negative 
population growth rates, and likely small and/or isolated populations 
at an increased risk of random genetic drift) are currently 
exacerbating the negative effects of the aforementioned threats, 
placing this species in danger of extinction. We also found no evidence 
of protective efforts for the conservation of Brazilian guitarfish that 
would reduce the level of extinction risk faced by the species. We 
therefore propose to list the Brazilian guitarfish as an endangered 
species.

Smoothhound Sharks

    Smoothhound sharks are members of the family Triakidae and genus 
Mustelus. The Mustelus species are often difficult to distinguish due 
to their conserved morphology and highly variable intraspecific 
meristic characteristics. This problem is compounded in the 
southwestern Atlantic, with very few specimens, particularly of larger 
individuals, leading to a lack of comparative ontogenetic observations 
that can be used for species diagnosis (Rosa and Gadig 2010). To date, 
there are at least five species of the genus Mustelus that occur with 
overlapping ranges in the southwestern Atlantic: M. canis, M. higmani, 
M. norrisi, M. fasciatus and M. schmitti (Rosa and Gadig 2010). Two of 
these species, M. fasciatus and M. schmitti, are elasmobranchs that are 
being considered for listing in this finding.

Striped Smoothhound Shark (Mustelus fasciatus)

Species Description

    The striped smoothhound is one of the most distinctive Mustelus 
species. Its head is large, with very small eyes and a sharply pointed 
snout (Compagno 1984; Rosa and Gadig 2010). Labial folds are present, 
and are longer on the upper jaw than on the lower jaw (Heemstra 1997; 
Rosa and Gadig 2010). The striped smoothhound's teeth are small and 
uniform in size and are similar in adults and juveniles (Heemstra 1997; 
Vooren and Klippel 2005b; Rosa and Gadig 2010). The first dorsal fin is 
short, broad, and triangular with a large base and is located closer to 
the pelvic fins than the pectoral fins (Compagno 1984; Rosa and Gadig 
2010). The second dorsal fin base is generally slightly smaller than 
the first dorsal fin base, and a dermal ridge is present between the 
two fins (Vooren and Klippel 2005b). The pectoral and pelvic fins have 
posterior margins that are nearly straight, and the caudal fin is not 
well developed, with a small and rounded ventral lobe (Rosa and Gadig 
2010). The striped smoothhound is grey or grey-brown on its dorsal side 
and white on its ventral side (Compagno 1984). Newborns and juveniles 
have dark bars of irregular widths running across the dorsal surface of 
their head and body (Heemstra 1997). The distinguishing vertical bars 
are still present in adults, but are not nearly as defined as they are 
in juveniles (Sadowski 1977; Heemstra 1997; Lorenz et al. 2010; Rosa 
and Gadig 2010). Overall, the striped smoothhound stands out from the 
other Mustelus species in the southwestern Atlantic because of its 
triangular dorsal and pectoral fins, underdeveloped caudal fin, unique 
tooth morphology, wide head, and small eyes (Rosa and Gadig 2010).

Range and Habitat Use

    The striped smoothhound is a demersal shark species, found at 
depths between 1 m and 250 m along the continental shelf and slope of 
the Southwestern Atlantic in Brazil, Uruguay, and Argentina (Soto 
2001). The species has a very restricted coastal distribution, ranging 
from Santa Catarina in southern Brazil to Bah[iacute]a Blanca in Buenos 
Aires Province, Argentina, which covers about 1,500 km of coastline 
(Lopez Cazorla and Menni 1983; Vooren and Klippel 2005b; Lorenz et al. 
2010). During the winter, adult biomass is concentrated on the 
Plataforma Sul between Rio Grande and Chu[iacute] off Rio Grande do 
Sul, Brazil (Vooren 1997; Vooren and Klippel 2005b). During the summer, 
a portion of the population migrates from Brazil to Uruguay and 
Argentine waters, while the rest of the population remains on the 
Plataforma Sul off Rio Grande do Sul as year-round residents (Vooren 
1997; Vooren and Klippel 2005b). Outside of Brazil, the striped 
smoothhound occurs only occasionally, with sporadic observations from 
the Mar del Plata, Argentina, near the southern boundary of its range 
(Lopez Cazorla and Menni 1983).
    Striped smoothhounds display clear ontogenetic (i.e., life-stage 
based) depth distributions. In Rio Grande do Sul, neonates are common 
in inshore areas between Cassino Beach and Chu[iacute] in depths less 
than 20 m, with the greatest frequencies between 2 m-5 m depth from 
November to January (summer months; Vooren and Klippel 2005b). As such, 
these shallow areas likely function as important nursery areas for the 
species (Vasconcellos and Vooren 1991; Soto 2001; Vooren and Klippel 
2005b). Adults are found mainly in water depths between 50 m-100 m in 
autumn and winter but move to shallower depths (<=50 m) in spring and 
summer (Vooren and Klippel 2005b). In the summer, males are much more 
common at depths between 20 m and 50 m, and are only rarely caught in 
waters less than 20 m deep, whereas females can be found in waters less 
than 20 m deep as they move into coastal waters for pupping during the 
summer months (Vooren and Klippel 2005b). Striped smoothhound are 
generally found in cooler water temperatures (11 [deg]C-15 [deg]C for 
juveniles during winter months, and >16 [deg]C for adults; Vooren and 
Klippel 2005b) and prefer water salinities between 33.3 ppt and 33.6 
ppt (Lopez Cazorla and Menni 1983).

Diet and Feeding

    Knowledge of the striped smoothhound's diet is limited. Soto (2001) 
studied the stomach contents of 17 specimens captured off Parcel da 
Solid[atilde]o in Rio Grande do Sul, Brazil. Crustaceans were the most 
abundant prey group, making up 82.4 percent of the diet, while fishes 
and mollusks were present in lower numbers (11.8 percent and 5.9 
percent, respectively). Box crabs (Heptus pudibundus) were the most 
prevalent crustacean, occurring in 52.9 percent of the stomachs 
examined (Soto 2001).

Growth and Reproduction

    There is scant information on striped smoothhound life history. Age 
and growth studies are not available and conflicting data exist for 
sizes at birth and maturity in Rio Grande do Sul. For example, one 
study reported that size at birth is between 39 cm and 43 cm TL, and 
that sexual maturity is reached at 130 cm and 135 cm TL for males and 
females, respectively (Vasconcellos and Vooren 1991). More recent 
studies report smaller sizes, with birth estimated between 35 cm and 38 
cm TL and size at maturity estimated at 119 cm TL for males and 121 cm 
TL for females (Soto 2011; Vooren and Klippel 2005b). The smaller size 
at maturity seen in the more recent studies could be a

[[Page 76081]]

compensatory response to the high levels of fishing mortality the 
species has experienced since the early 1980s (see Overutilization for 
Commercial, Recreational, Scientific or Educational Purposes section). 
The maximum observed sizes for striped smoothhound are 162 cm TL (17.5 
kg) for males and 177 cm TL (29.7 kg) for females (Lorenz et al. 2010).
    Striped smoothhound have placental viviparous reproduction (Vooren 
1997) and a gestation period that lasts between 11 and 12 months (Soto 
2001; Lorenz et al. 2010). Pregnant females migrate into shallow waters 
(<20 m) along the Rio Grande do Sul coast to give birth from October to 
December (Vasconcellos and Vooren 1991; Vooren 1997; Lorenz et al. 
2010). Vooren and Klippel (2005b) report that pupping takes place from 
November to January, but Soto (2001) reports that it occurs earlier, 
from September to November. Striped smoothhounds have 4-14 pups per 
litter, with an average of 8 pups (Vasconcellos and Vooren 1991). 
Newborns are seen in high frequency in November, along with females 
with mature follicles and postpartum uteri, suggesting an annual 
reproductive cycle (Vasconcellos and Vooren 1991). After pupping, 
females move to deeper waters to mate (Soto 2001; Vooren and Klippel 
2005b; Lorenz et al. 2010). One study found a positive relationship of 
litter size and maternal size (Soto 2001); however, two other studies 
found no correlation (Vasconcellos and Vooren 1991; Heemstra 1997).

Genetics and Population Structure

    Studies examining the genetics of the species or information on its 
population structure could not be found.

Demography

    The striped smoothhound is generally thought to have low fecundity, 
with a long gestation time (~1 year), and an average of only eight pups 
(range = 4-14 pups). Information regarding natural mortality rates or 
the intrinsic rate of population increase (r) of the striped 
smoothhound is unavailable; however, based on the life history 
parameters described previously, the species likely has low 
productivity, which may hinder its ability to recover from 
exploitation.

Historical and Current Distribution and Population Abundance

    The striped smoothhound is distributed from Santa Catarina in 
southern Brazil to the Bah[iacute]a Blanca in Buenos Aires Province, 
Argentina. While striped smoothhound were once considered a dominant 
permanent resident in Rio Grande do Sul in the early 1970s and 1980s, 
and displayed predictable abundance changes throughout the year (Vooren 
1997), they are now considered sporadic in this area and rare in the 
northern and southern portions of their range (Soto 2001). Prior to 
fisheries exploitation, it is thought that the striped smoothhound had 
naturally low abundance based on their relatively low frequency of 
occurrence in fishery research surveys (Vooren and Klippel 2005b). For 
example, in research trawl surveys on the Plataforma Sul, conducted 
from 1972-2005 with over 1,500 hauls, striped smoothhound occurred at a 
frequency of only 10 percent in the trawl hauls from the 10 m-100 m 
depth range (Vooren and Klippel 2005b) and comprised only 2 to 4 
percent of the total elasmobranch CPUE for the period of 1980-1984. 
Despite this low frequency of occurrence, Vooren and Klippel (2005b) 
note that neonates of the species were relatively abundant in the 1980s 
in the summer and commonly observed along the 10,688 km of the Rio 
Grande do Sul coastline. In fact, for the period of 1981-1985, 
estimated CPUE from artisanal fisheries operating off Rio Grande do Sul 
ranged from 1.9 individuals/haul for beach seines to 18.5 individuals/
haul for gillnet fishing gear. In research trawl surveys conducted in 
shallow waters of 10 m-20 m depths in 1981 and 1982, juvenile M. 
fasciatus occurred at a frequency of 54-86 percent in trawl hauls with 
a CPUE of 2.55-3.95 kg/hour. However, in follow-up surveys conducted 
nearly two decades later, juveniles and neonates were mostly absent 
from hauls, despite significant sampling in habitats where they had 
been known to occur. In 2005, neonates were noted as abundant along 
only 395 km of the Rio Grande do Sul coastline, corresponding to an 
estimated 95 percent decline in occupied area by neonates between 1981 
and 2005 (Vooren and Klippel 2005b).
    In Uruguay and Argentina, current catches by fishermen are 
infrequent. Additionally, trawl surveys conducted along the coastal 
region of the Bonaerensean (Buenos Aires) District of northern 
Argentina and Uruguay indicate a 96 percent decline in biomass of the 
species between 1994 and 1999 (Hozbor et al. 2004). Striped 
smoothhounds were also absent from Argentine research surveys conducted 
in the 1990s and are currently rarely caught by the commercial fleet, 
suggesting that the Argentine sea represents the periphery of its 
distribution (Massa 2013).

Summary of Factors Affecting Striped Smoothhound (Mustelus fasciatus)

    We reviewed the best available information regarding historical, 
current, and potential threats to the striped smoothhound species. We 
find that the main threat to this species is overutilization for 
commercial purposes. We consider the severity of this threat to be 
exacerbated by the species' natural biological vulnerability to 
overexploitation, which has led to significant declines in abundance of 
all life stages, particularly neonates. We find current regulatory 
measures inadequate to protect the species from further 
overutilization. Hence, we identify these factors as additional threats 
contributing to the species' risk of extinction. We summarize 
information regarding these threats and their interactions below 
according to the factors specified in section 4(a)(1) of the ESA. 
Available information does not indicate that habitat destruction, 
modification or curtailment, disease, predation or other natural or 
manmade factors are operative threats on these species; therefore, we 
do not discuss these factors further in this finding. See Casselbury 
and Carlson (2015c) for discussion of these ESA Section 4(a)(1) threat 
categories.

Overutilization for Commercial, Recreational, Scientific, or 
Educational Purposes

    The greatest threat to striped smoothhound is overutilization in 
commercial fisheries, particularly by those fisheries operating on the 
Plataforma Sul off Rio Grande do Sul. The Plataforma Sul comprises 
approximately one-third of the species' geographic distribution and is 
the area where the species was historically most concentrated. In fact, 
striped smoothhound were commonly caught as bycatch in the 1970s and 
1980s on the Plataforma Sul in Brazil, albeit in low numbers (Soto 
2001; Vooren and Klippel 2005b). Estimates of CPUE of M. fasciatus on 
the shelf in the early 1980s varied between 2 kg/hr and 7 kg/hr (in 
areas of low density) and 8 kg/hr to 33 kg/hr (in areas where the 
species was more highly concentrated) (Vooren and Klippel 2005b). 
Although the presumed naturally low abundance of striped smoothhound 
prohibited a directed fishery from developing for this species on the 
Plataforma Sul, they were and continue to be caught as part of the 
multispecies smoothhound fisheries and as bycatch in fisheries for 
other species such as drums, flounders, and mullets (Haimovici and 
Mendon[ccedil]a 1996; Vooren and Klippel 2005b). Striped

[[Page 76082]]

smoothhounds have been reported in landings from the industrial pair 
and double-rig trawl fleets, bottom longline and gillnet fleets and 
artisanal fisheries (Mazzoleni and Schwingel 1999). When caught, large 
striped smoothhound weighing more than 4 kg are generally retained and 
those less than 4 kg are discarded (Haimovici and Maceira 1981), but 
the rate of discard mortality is unknown. However, as both industrial 
and artisanal fishing intensified on the Plataforma Sul in the 1980s 
and continued through the 1990s, with the heavy use of trawls, gillnets 
and beach seines within the habitat of the striped smoothhound shark, 
the rates of fishery-related mortality experienced by the species 
clearly led to dramatic declines in its abundance (Soto 2001; Hozbor et 
al. 2004).
    The intense coastal commercial and artisanal fishing off Rio Grande 
do Sul that takes place in nearshore waters along the coast (see 
additional discussion of these fisheries in the Brazilian guitarfish 
assessment) has likely had, and continues to have, the greatest impact 
on the species. These coastal fisheries primarily use beach seines, 
gillnet and trawl gear in the nearshore locations where striped 
smoothhound neonates and juveniles are found year-round. This level of 
fishing effort exerts constant pressure on the species before it 
reaches maturity (Soto 2001; Vooren and Klippel 2005b), and 
consequently, affects the recruitment of juvenile sharks into the 
population (Vooren 1997). Significant declines in neonate and juvenile 
populations have already been observed. Between the areas of 
Chu[iacute] and Torres of Rio Grande do Sul, Brazil, for example, 
neonates were abundant in the summer in the 1980s, along the coast from 
depths of 2 m-20 m, representing an area of occupancy of about 10,688 
km\2\. According to Hozbor et al. (2004), gillnets set off beaches in 
this area would capture neonate striped smoothhound in large numbers 
(10-100 per set) in the 1980s; however, by 2003, this level of removal 
had led to substantial declines in the population, with striped 
smoothhound currently caught only sporadically and in much smaller 
numbers. Similarly, off of Cassino Beach (located close to the mid-
point between Chu[iacute] and Torres) Vooren and Klippel (2005b) 
estimated that CPUE of neonate striped smoothhound decreased by up to 
99 percent in the artisanal fisheries during this time period. 
Specifically, the CPUE of neonate striped smoothhound and frequency of 
its occurrence in the artisanal gillnet fishery sets went from 18.5 
(individuals/set) and 75 percent, respectively, in 1981-1985 to 0.2 
(individuals/set) and 13 percent in 2002-2003. In 2005, neonates 
remained common only in the inner edge of their former 10,688 km\2\ 
occupied area, in depths between 2 m-5 m: An area of only 395 km\2\. 
This significant reduction in occupied area translates to an estimated 
95 decline in neonate production and is likely a result of the intense 
artisanal and industrial fishing pressure and overutilization of the 
species within this area. Trawl surveys conducted in the same area but 
in depths of 10 m-20 m showed a similar decline in the CPUE of juvenile 
striped smoothhounds, from 2.55 kg/hour in 1981 and 3.95 kg/hour in 
1982 to 0.02 kg/hour in 2005, an estimated 99 percent decrease in 
abundance (Vooren and Klippel 2005b).
    In addition to the coastal artisanal and industrial fisheries, the 
intense fishing by the Plataforma Sul trawl fisheries that operate 
between the coastal waters and inner continental shelf (see description 
of the pair trawl fleet in the Brazilian guitarfish assessment) also 
affected and continues to impact the reproductive capacity of the 
striped smoothhound population in southern Brazil. These trawl 
fisheries, whose area of operation intersects with the spring migration 
of female M. fasciatus, incidentally catch both pregnant females and 
adult male striped smoothhounds on the inner shelf (Haimovici and 
Mendon[ccedil]a 1996; Vooren and Klippel 2005b). As such, all life-
stages of the species as well as both sexes are subject to constant 
fishing pressure year-round, which Vooren and Klippel (2005b) point to 
as the primary cause for the significant decline and present rarity of 
the resident striped smooth population on the Plataforma Sul. As 
discussed in the Brazilian guitarfish assessment, fishing by the 
industrial and artisanal fleets continues to occur at high efforts on 
the Plataforma Sul and especially within the important coastal nursery 
and inner shelf habitats for the species (which overlap with R. 
horkelli). In fact, total marine fish landings from Rio Grande do Sul 
(where striped smoothhound are most concentrated on the Plataforma Sul) 
have increased substantially in recent years, from 23,594 t in 2007 to 
34,385 t in 2011 (an increase of 46 percent over 4 years) (MMA/IBAMA 
2007; IBAMA/CEPERG 2012). Out of the 27 Brazilian States, Rio Grande do 
Sul reports the 6th highest level of marine fish landings and Santa 
Catarina (which represents the northern periphery of the species' range 
in Brazil) reports the highest level of marine fish landings (121,960 t 
in 2011) (IBAMA/CEPERG 2012). Based on the trends in the available 
fishing data, it is unlikely that the industrial and artisanal fishing 
on the Plataforma Sul, and particularly off the coast of Rio Grande do 
Sul within striped smoothhound habitat, will decrease in the 
foreseeable future, indicating that overutilization (in the form of 
bycatch mortality) is still a threat to the species.
    Outside of Brazil, off Uruguay and Argentina, striped smoothhound 
are caught sporadically as bycatch in gillnets, bottom longlines, and 
trawls in fisheries targeting Brazilian flathead (Percophis 
brasiliensis), Argentinian sandperch (Pseudopercis semifasciata), apron 
rays (Discopyge tschudii), striped weakfish (Cynoscion guatucupa) and 
whitemouth croaker (Micropogonias funieri) (Chiaramonte 1998; Lasta et 
al. 1998; Domingo et al. 2008). Bycatch levels and the associated 
fishery-related mortality of striped smoothhound in these fisheries 
have resulted in marked declines in the population, with trawl surveys 
conducted in the coastal region of the Bonaerensean District of 
northern Argentina and Uruguay indicating a 96 percent decline in the 
biomass of striped smoothhound between 1994 and 1999 (Hozbor et al. 
2004). In the early 2000s, annual landings of smoothhounds (primarily 
M. schmitti, but also M. fasciatus and M. canis) in Uruguay increased 
dramatically, from fewer than 350 t in the 1990s to a peak of 1,300 t 
in 2000 and remained above 1,000 t through 2005; however, the cause for 
this reported increase in landings is unknown and, since 2000, landings 
have progressively declined (Domingo et al. 2008). In Uruguay's latest 
2013 Fishery Statistics Bulletin, there were no reported landings of M. 
fasciatus (Direcci[oacute]n Nacional de Recursos Acu[aacute]ticos 
(DINARA) 2014). Similarly, in Argentina, striped smoothhounds are also 
currently a rare occurrence (Casselberry and Carlson 2015c).

Inadequacy of Existing Regulatory Mechanisms

    Like the daggernose shark and Brazilian guitarfish, the striped 
smoothhound is also listed as critically endangered under Annex I of 
Brazil's endangered species list. Aside from authorized conservation 
research purposes, the capture, transport, storage, and handling of 
striped smoothhounds is prohibited. There is also a prohibition of 
trawl fishing within three nautical miles of the coast of southern 
Brazil, although the enforcement of this prohibition has been noted as 
difficult

[[Page 76083]]

(Chiaramonte and Vooren 2007). In addition, the species is still 
susceptible to being caught as bycatch in the legally permitted coastal 
gillnet fisheries and offshore trawl and gillnet fisheries and 
vulnerable to the associated bycatch mortality (Lessa and Vooren 2007). 
While the striped smoothhound is not listed as one of the 12 species of 
concern under Brazil's FAO NPOA-sharks, the plan does call for a 
fishing exclusion area over a large region of the coast of Rio Grande 
do Sul at depths of 20 m to protect nursery areas (which would include 
the striped smoothhound nursery habitat) (Lessa et al. 2005). The plan 
also proposes a fishing closure between 32[deg] S. and 34[deg] S., 
where adults of the species now seem to be found in greatest abundance 
(Vooren and Klippel 2005b). However, as mentioned previously, the plan 
was only just approved as of December 2014, and will not be fully 
implemented for another 5 years. Thus, the implementation and 
effectiveness of the recommendations outlined in the plan remain 
uncertain, with the best available information indicating that current 
regulatory measures in Brazil to protect vulnerable species are poorly 
enforced.
    In contrast to Brazil, Uruguay's FAO NPOA-sharks does list the 
striped smoothhound as a species of high priority (Domingo et al. 
2008), and, as stated previously, has set goals to collect the 
necessary information on its priority species in order to conduct 
abundance assessments, review current fishing licenses, and promote 
public awareness to release captured individuals. However, no updated 
results from the goals and priorities of this plan could be found. As 
such, their implementation and overall effectiveness at decreasing the 
threats to the striped smoothhound remains highly uncertain. 
Additionally, in 2013, the National Directorate of Aquatic Resources 
(DINARA), the state agency responsible for regulating and controlling 
fishing and aquaculture in Uruguay, passed a resolution authorizing 
fishing with gillnets and longlines in the Rio de la Plata and Atlantic 
Ocean at a distance less than 300 m from the coast, between March 1 and 
October 31 of each year. This type of fishing was previously prohibited 
in 2008; however, due to concerns brought forth by the artisanal 
fishermen, primarily of the socio-economic nature, DINARA revised the 
prohibition to allow for this seasonal fishing (Resolution No. 24/04/
2013 MGAP). Although this seasonal restriction should provide some 
protection for the population of migrating pupping females (which moves 
inshore to pup primarily from October to December), it does little to 
decrease fisheries-related mortality of young striped smoothhounds 
which remain in these coastal waters following birth. In other words, 
given that the depth distribution of M. fasciatus extends from shallow 
coastal waters out to 100 m depths, and fishery records from Uruguay 
show that the species is primarily bycaught in the artisanal longline 
and gillnet fisheries (Domingo et al. 2008), this new resolution is 
unlikely to adequately decrease the threat of overutilization to 
striped smoothhounds.

Extinction Risk

    The best available information provides multiple lines of evidence 
indicating that the M. fasciatus currently faces a high risk of 
extinction. Below, we present the demographic risk analysis, threats 
assessment, and overall risk of extinction for the striped smoothhound 
shark.

Demographic Risk Analysis

Abundance
    While there are no quantitative abundance estimates available for 
M. fasciatus, qualitative information and historical catch data can 
provide some insight into the current abundance of the species. Based 
on data from research trawl surveys, it is thought that the striped 
smoothhound naturally occurred at low abundance before they were 
exploited in fisheries (Vooren and Klippel 2005b), and were once 
considered a dominant permanent resident species on the Plataforma Sul. 
However, presently, the species is rarely observed anywhere in its 
range and caught only sporadically. Historical data from artisanal 
gillnet and beach seine fisheries suggest neonate production on the 
Plataforma Sul has decreased by 95 percent since the 1980s. 
Additionally, research trawl survey data estimate a decline in juvenile 
striped smoothhounds in these coastal waters of around 99 percent over 
this same period. Considering adult female striped smoothhounds follow 
a spring migration into these same coastal areas for pupping purposes, 
and, thus, are also susceptible to these artisanal fisheries, the 
significant declines in neonate and juvenile abundance likely 
correspond to declines in the number of reproductively active females 
in the population as well, as overutilization of the species through 
the direct removal of young striped smoothhound shark recruits.
    Although CPUE data are lacking from other parts of the species' 
range, with catches of striped smoothhound characterized as sporadic 
and rare in Uruguay and Argentina, respectively, survey data suggest 
that the migratory population has also experienced similar declines. 
Based on trawl survey data collected from along the Bonaerensean 
District of northern Argentina and Uruguay, the population of striped 
smoothhounds suffered an estimated 96 percent decline in biomass 
between 1994 and 1999. No other information on abundance or trends was 
available from this portion of the species' range. However, considering 
the species was of naturally low abundance prior to exploitation, and 
fishing pressure has historically been high (particularly on neonates 
in nursery areas and juvenile and adults on the inner shelf, including 
on both the resident and migratory populations) with no indications 
that this pressure has ceased, it is likely that the species has 
continued to suffer declines throughout its range.
Growth Rate/Productivity
    Very little information is known about the life history of M. 
fasciatus. Age and growth studies are unavailable for the species, and 
there is conflicting information reported from the literature regarding 
the species' size at birth and size at maturity from Rio Grande do Sul, 
Brazil. Estimates of size at maturity range from 119 to 130 cm TL for 
males and 121 to 135 cm TL for females, with the smaller and more 
recent size estimates a possible compensatory response to fishing 
mortality. Size at birth ranges from 35 to 48 cm TL. The species is 
generally thought to have low fecundity, with a long gestation time (~1 
year) and an average of only 8 pups per litter. These reproductive 
characteristics suggest the species has relatively low productivity, 
similar to other elasmobranch species, which has likely hindered its 
ability to quickly rebound from threats that decrease its abundance 
(such as overutilization).
Spatial Structure/Connectivity
    The striped smoothhound has a very restricted coastal range of only 
1,500 km. On the Plataforma Sul off southern Brazil, there is thought 
to be a permanent, year-round resident population. Vooren and Klippel 
(2005b) note that the area occupied by this population represents one 
third of the species' total range, and that the conservation of this 
resident population is integral to the conservation of the taxon as a 
whole, indicating the relative importance of this population to the 
species' survival. However, there is also thought to be a migratory 
population that is present on the Plataforma Sul in the winter that 
returns to Uruguay and

[[Page 76084]]

Argentina in the summer concurrent with changes in water temperature. 
No information exists on the connectivity between the resident and 
winter migrant M. fasciatus populations found on the Plataforma Sul; 
however, based on the significant decline of the population off the 
Buenos Aires Province, it seems likely that the increased fishing 
pressure on the migratory population while they winter on the 
Plataforma Sul may be negatively impacting the populations found in 
other parts of the species' range.
Diversity
    The loss of diversity can increase a species' extinction risk 
through decreasing a species' capability of responding to episodic or 
changing environmental conditions. This can occur through a significant 
change or loss of variation in life history characteristics (such as 
reproductive fitness and fecundity), morphology, behavior, or other 
genetic characteristics. Although it is unknown if M. fasciatus has 
experienced a loss of diversity, high fishing pressure on neonates and 
reproductively active adults in coastal waters has negatively affected 
recruitment rates of neonates into the population, resulting in a 
significant depletion of the resident population on the Plataforma Sul. 
This reduction of the important resident population in Brazil, combined 
with the likely small populations elsewhere throughout its range, 
suggest the species may be at an increased risk of random genetic drift 
and could experience the fixing of recessive detrimental genes, 
reducing the overall fitness of the species.

Threats Assessment

    The primary threat to striped smoothhounds is overutilization in 
commercial fisheries. Although not targeted in any fisheries throughout 
its range, due to its presumed naturally low abundance, striped 
smoothhounds are caught as part of the multispecies smoothhound 
fisheries and as bycatch in fisheries for other species such as drums, 
flounders, and mullets. While adult striped smoothhounds were once 
commonly caught as bycatch in the 1970s and 1980s in Brazil, albeit in 
low numbers, they are now considered rare in commercial catches. 
Additionally, intensive fishing by gillnet and trawl fisheries in 
shallow coastal areas where juveniles and neonates occur results in 
constant fishing pressure on the species before it reaches maturity, 
negatively affecting recruitment of neonates into the population. In 
fact, the historical data on the abundance of newborns in coastal 
waters provide strong evidence that a 95 percent reduction in annual 
production of neonates occurred from 1984 to 2005 as a result of 
constant fishing pressure in important coastal nursery areas. Adult 
striped smoothhounds are also susceptible to these fisheries during 
their spring migration into these same coastal areas for pupping, and 
are at risk of being caught as bycatch by the industrial gillnet and 
trawl fleets operating on the inner shelf throughout the rest of year. 
In fact, the level of fishing mortality on the migratory wintering 
population on the Plataforma Sul may have led to the observed declines 
in the striped smoothhound population found off the coast of northern 
Argentina. Thus, the intense fishing effort by the commercial and 
artisanal fisheries on the Plataforma Sul appear to be negatively 
affecting the reproductive capacity and growth of the population 
throughout its range.
    In 2004, the species was listed on Brazil's endangered species 
list, which effectively prohibited the capture of this species. As of 
2014, the species was classified as ``critically endangered'' on this 
list. Although the species is not identified as one of 12 species of 
concern under Brazil's FAO NPOA-sharks, the plan calls for fishing 
closures in areas of <20 m deep that would provide protection to 
neonates and juveniles, as well as other closures to protect adult 
aggregations. In Uruguay, the striped smoothhound is listed as a 
species of high priority on its FAO NPOA-sharks (Domingo et al. 2008); 
however, as mentioned previously, the implementation and effectiveness 
of the recommendations outlined in both the Brazilian and Uruguayan 
plans remain uncertain, with the best available information indicating 
that current regulatory measures in both countries are inadequate to 
protect the species from further overutilization.
    Given the continued and significant fishing effort by the 
industrial trawl fleet and artisanal gillnet on the Plataforma Sul, 
contributing to the fishing mortality of the resident population as 
well as the wintering migratory population, and inadequacy of existing 
regulatory measures to control the exploitation of the marine resources 
throughout the species' range, the best available information suggests 
that overutilization of the species by industrial and artisanal 
fisheries is a threat significantly contributing to its risk of 
extinction.

Risk of Extinction

    Although there is significant uncertainty regarding the current 
status of the species, the best available information indicates that 
the species has suffered significant declines throughout its range due 
to overutilization in industrial and artisanal fisheries. The species' 
very restricted coastal range, with data to suggest it has undergone a 
decline of over 90 percent in one third of this range, combined with 
its present rarity throughout the rest of its range, make it 
particularly susceptible to local extirpations and significantly 
increases its risk of extinction from environmental and anthropogenic 
perturbations or catastrophic events. With no indication that abundance 
trends have stabilized or reversed in recent years, nor any indication 
that regulatory measures have been implemented or are adequately 
enforced to protect the Plataforma Sul neonates in important nursery 
areas, the local reproducing adult population, or the migratory 
population from unsustainable fishing mortality levels, it is likely 
that the species continues to suffer from population declines. Based on 
the species' demographic risks, these severely depleted populations are 
likely to be strongly influenced by stochastic or depensatory processes 
without adequate protection. This vulnerability is further exacerbated 
by the present threats of overutilization and inadequacy of existing 
regulatory measures that continue to contribute to the decline of the 
existing populations, compromising the species' long-term viability. 
Therefore, based on the best available information and the above 
analysis, we conclude that M. fasciatus is presently at a high risk of 
extinction throughout its range.

Protective Efforts

    With the exception of the recommendations within Brazil and 
Uruguay's FAO NPOA-sharks, we were unable to find any other information 
on protective efforts for the conservation of striped smoothhound 
sharks in Brazil, Uruguay, or Argentina that would potentially alter 
the extinction risk for the species. We seek additional information on 
other conservation efforts in our public comment process (see below).

Proposed Determination

    Based on the best available scientific and commercial information 
as presented in the status review report and this finding, we find that 
the striped smoothhound is presently in danger of extinction throughout 
its range. We assessed the ESA section 4(a)(1) factors and conclude 
that the species faces ongoing threats from overutilization and 
inadequacy of existing regulatory

[[Page 76085]]

mechanisms throughout its range. The species' natural biological 
vulnerability to overexploitation and present demographic risks (e.g., 
significantly reduced and declining abundance levels, decreases in 
neonate production and recruitment, low productivity, restricted range 
with likely small and/or isolated populations at an increased risk of 
random genetic drift) are currently exacerbating the negative effects 
of the aforementioned threats, placing this species in danger of 
extinction. We also found no evidence of protective efforts for the 
conservation of striped smoothhound that would reduce the level of 
extinction risk faced by the species or otherwise alter its current 
status. We therefore propose to list the striped smoothhound shark as 
an endangered species.

Narrownose Smoothhound Shark (Mustelus schmitti)

Species Description

    The narrownose smoothhound shark has a slender body, similar in 
form to other triakids, and a short head (Compagno 1984; Rosa and Gadig 
2010). The species has large eyes and a snout that is bluntly angular 
(Compagno 1984) with a narrow internostril distance (Rosa and Gadig 
2010). Like M. fasciatus, labial folds are present on the mouth and are 
longer on the upper jaw than on the lower jaw (Compagno 1984; Heemstra 
1997; Rosa and Gadig 2010). Narrownose smoothhounds are grey with 
numerous small white spots on their dorsal side and solid white 
coloration on their ventral side (Compagno 1984; Heemstra 1997). The 
trailing edges of both dorsal fins have exposed ceratotrichia (slender 
soft or stiff filaments of an elastic protein that superficially 
resembles keratin), a distinctive characteristic for the species (Rosa 
and Gadig 2010). The pectoral and pelvic fins are both relatively 
small, (Compagno 1984) and the ventral lobe of the caudal fin is poorly 
developed (Heemstra 1997).

Range and Habitat Use

    The narrownose smoothhound is found in the southwestern Atlantic 
from southern Brazil to southern Argentina between 22[deg] S. and 
47[deg]45' S. (Belleggia et al. 2012). Rio de Janeiro, Brazil, is the 
northernmost limit of the species' range (Oddone et al. 2007) and 
R[iacute]a Deseado, Argentina is the southernmost limit (Chiaramonte 
and Pettovello 2000). Narrownose smoothhound occurs at depths up to 120 
m in Argentina and has been captured as deep as 195 m in Brazil 
(Belleggia et al. 2012). In Argentinian waters, narrownose smoothhound 
is found in waters with surface temperatures of 8 [deg]C-11.7 [deg]C 
and bottom temperatures of 5.5 [deg]C-11 [deg]C (Menni 1985; 
Chiaramonte and Pettovello 2000) and salinity that is generally 22.4 
practical salinity units (psu) and higher (Molina and Cazorla 2011).
    Like striped smoothhounds, a portion of the narrownose smoothhound 
population is migratory. In the winter, juveniles, adults, and gravid 
females migrate north into Brazilian waters and remain there from April 
to November (Haimovici 1997; Vooren 1997; Oddone et al. 2005; Massa et 
al. 2006). This migration is thought to be triggered by cold water 
moving north into their Argentinian range (Haimovici 1997). Water 
temperatures in the wintering grounds are usually between 12 [deg]C and 
20 [deg]C (Massa et al. 2006). In the spring, summer, and autumn 
(December to April) narrownose smoothhounds are most common in waters 
off Uruguay (Vooren 1997; Oddone et al. 2005) and Argentina, with 
highest abundance in Argentinian waters noted off Buenos Aires Province 
and northern Patagonia (Molina and Cazorla 2011).

Diet and Feeding

    Olivier et al. (1968) first characterized the diet of the 
narrownose smoothhound as carcinophagous (i.e., eats crabs and other 
crustaceans), benthic infaunal (i.e., eats animals that live in the 
substrate), and ichthiophagous (i.e., eats fish). The narrownose 
smoothhound is an opportunistic predator that generally feeds on 
epifaunal benthic organisms and the diet appears to vary geographically 
and ontogenetically (Capitoli et al. 1995). For example, in R[iacute]o 
de la Plata and El Rinc[oacute]n, Argentina, the diet is generally 
dominated by crustaceans, fishes, and polychaetes; however, as 
narrownose smoothhounds increase in body size, the consumption of 
polychaetes declines and is replaced by more fishes and crustaceans. 
The shift to crustaceans occurs around 60 cm TL, while narrownose 
smoothhounds around 85 cm TL feed primarily on fish (Belleggia et al. 
2012). Temporal and ontogenetic variations in diet were also found for 
M. schmitti in Anegada Bay, Argentina, where neonates are more 
specialized feeders and predominantly consume decapods, and adults more 
commonly consume polychaetes, decapods, bivalves, and occasionally 
cephalopods (Molina and Carzorla 2011). Smaller scale diet studies in 
Argentina also found the diet to be dominated by epifaunal benthic 
organisms, including decapod crabs, fishes, isopods, and polychaetes, 
and, to a lesser extent, some teleosts and cephalopods (Chiaramonte and 
Pettovello 2000; Van der Molen and Caille 2001).

Growth and Reproduction

    The narrownose smoothhound has an estimated lifespan of 20.8 and 
24.7 years for males and females, respectively (Hozbor et al. 2010). In 
general, narrownose smoothhound females grow faster and grow to a 
larger size than males (Chiaramonte and Pettovello 2000; Sidders et al. 
2005; Segura and Milessi 2009). Maximum recorded size for M. schmitti 
is 110 cm TL, with a modal TL in Brazil of 60 cm for males and 72 cm 
for females ((Massa et al. 2006; Molina and Cazorla 2011). Size at 
maturity varies throughout the narrownose smoothhound's range, with 
estimates for male size at 50 percent maturity ranging from 55 cm TL to 
59 cm TL and for females ranging from 56 to 72 cm TL (Chiaramonte and 
Pettovello 2000; Oddone et al. 2005; Segura and Milessi 2009; Colautti 
et al. 2010). Age at first breeding in Brazil is 4 years for females 
and 3 years for males, while it is 6.5 years for females and 5.7 years 
for males in Argentina (Casselberry and Carlson 2015d).
    Narrownose smoothhound sharks are non-placental and reported to be 
yolk-sac viviparous (Hamlett et al. 2005; Gal[iacute]ndez et al. 2010). 
Their reproductive cycle is annual with a gestation of 11 months 
followed by immediate ovulation and mating (Chiaramonte and Pettovello 
2000). In the spring, females move inshore to pup and mate, and then 
migrate offshore in late summer to early autumn (Colautti et al. 2010). 
Reproduction occurs at different times, ranging from late November in 
northern Argentina to mid-December at the southern extent of its range 
(Molina and Cazorla 2011). Litter size varies between 2 and 14 pups 
(Massa et al. 2006), with an average litter size of around 4 to 5 pups 
(Sidders et al. 2005; Gal[iacute]ndez et al. 2010). Litter size 
increases significantly with maternal length (Oddone et al. 2005; 
Cort[eacute]s 2007), but larger females do not produce larger offspring 
(Sidders et al. 2005). Nursery grounds for the narrownose smoothhound 
shark in Argentina (based on higher abundance of neonates and juveniles 
within these areas) are found in the El Rinc[oacute]n area (including 
Bah[iacute]a Blanca and Anegada Bay) and the R[iacute]o de la Plata 
(including Samboromb[oacute]n Bay) (Chiaramonte and Pettovello 2000; 
Molina and Cazorla 2011).

[[Page 76086]]

Genetics and Population Structure

    In terms of population structure, only one genetics study has been 
conducted to determine if multiple stocks occur throughout the species' 
range (Pereya et al. 2010). Results of this study indicate that M. 
schmitti comprises a single demographic unit in the R[iacute]o de la 
Plata area and its maritime front (area separating Uruguay and 
Argentina), suggesting high connectivity and genetic homogeneity over 
this geographic range (Perey et al. 2010). The authors attribute this 
genetic homogeneity to the likely high dispersal and migration rates of 
the species (based on tagging studies of related species M. antarcticus 
and M. lenticulatis; Francis 1988) and lack of obvious dispersal 
barriers in the study area. The study also found that nucleotide 
diversity in M. schmitti was lower than that reported for other 
elasmobranchs. These results may indicate that narrownose smoothhound 
experienced a genetic bottleneck, recent expansion, or selection, which 
potentially occurred during the Pleistocene Era (Pereyra et al. 2010).

Demography

    The annual population growth rate for narrownose smoothhound in 
Brazil was calculated to be 1.058 between 1980 and 1994 (Massa et al. 
2006). More recently, using life history parameters from individuals 
collected off Mar del Plata, Argentina, Cort[eacute]s (2007) determined 
the intrinsic rate of increase (r) for narrownose smoothhound to be 
0.175 per year when the population is not subject to exploitation 
(lower 95 percent confidence limit = 0.030; upper 95 percent confidence 
limit = 0.314). Because of this relatively high intrinsic rate of 
increase, Cort[eacute]s (2007) concluded that narrownose smoothhound 
could withstand higher levels of exploitation than other coastal sharks 
in the Buenos Aires coastal region, with sustainable exploitation rates 
equivalent to an annual removal rate of about 10 percent of the 
population. Natural mortality rates of the species ranged from 0.139 to 
0.412 (Cort[eacute]s 2007). These demographic parameters place 
narrownose smoothhound toward the faster growing end of the ``fast-
slow'' continuum of population parameters calculated by Cort[eacute]s 
(2002), which means this species generally has a higher potential to 
recover from exploitation.

Historical and Current Distribution and Population Abundance

    The narrownose smoothhound is the most abundant and widely 
distributed triakid in the Argentine Sea (Van der Molen and Caille 
2001), with densities off Rio de la Plata as high as 44 t/nm\2\ in 1994 
(Cousseau et al. 1998). Throughout the rest of the Argentine-Uruguayan 
Common Fishing Zone (AUCFZ) [an area that extends 200 nm off the coast 
from the border of Uruguay and Brazil to just south of Necochea, 
Argentina)] densities of narrownose smoothhounds ranged between 1 and 
10 t/nm\2\, with some areas supporting densities as high as 22 t/nm\2\ 
(Cousseau et al. 1998). Based on data from research surveys conducted 
in the spring in Argentine maritime waters (covering coastal Buenos 
Aires and waters off Uruguay from 35[deg] S.-41[deg] S.), abundance of 
M. schmitti in this area increased from 82,000 t in 1978 to 184,302 t 
in 1994. In 1999, M. schmitti abundance on the continental shelf and 
slope from 34[deg] S.-48[deg] S. was estimated to be 191,722 t 
(Argentina FAO NPOA-sharks 2009). Although recent abundance estimates 
could not be found, Massa et al. (2006), citing unpublished data, 
indicate that between 1998 and 2002, biomass of the species declined by 
22 percent in main fishing areas along the coast of Buenos Aires 
Province (Argentina) and the Bonaerensean region (Uruguay) and national 
landings in Argentina decreased by 30 percent. By 2003, abundance of M. 
schmitti (between 35[deg] S.-41[deg] S.) had fallen to 88,500 t 
(Argentina FAO NPOA-sharks 2009). Declines in abundance continued to be 
seen in Argentine waters through 2005 (Massa and Hozbor 2008). 
Similarly, in Brazil, based on CPUE data, abundance of the winter 
migrant population of M. schmitti is estimated to have declined by 85 
percent between 1985 and 1994 (Miranda and Vooren 2003), and Massa et 
al. (2006) note that a small local breeding population that was 
relatively common in the 1980s in southern Brazil has seemingly been 
extirpated from the area.

Summary of Factors Affecting Narrownose Smoothhound (Mustelus schmitti)

    We reviewed the best available information regarding historical, 
current, and potential threats to the narrownose smoothhound shark. We 
find that the main threat to this species is overutilization for 
commercial purposes. We consider the severity of this threat to be 
reduced by the species' natural biological ability to withstand higher 
levels of exploitation. However, we find that historical and present 
levels of utilization have exceeded the species' biological capacity to 
quickly recover from exploitation, and have subsequently led to 
significant declines in abundance. We also find that current regulatory 
measures are inadequate to protect the species from further 
overutilization. Hence, we identify these factors as additional threats 
contributing to the species' risk of extinction. We summarize 
information regarding these threats and their interactions below 
according to the factors specified in section 4(a)(1) of the ESA. 
Available information does not indicate that habitat destruction or 
modification, disease, predation or other natural or manmade factors 
are operative threats on these species; therefore, we do not discuss 
these factors further in this finding. See Casselbury and Carlson 
(2015d) for discussion of these ESA section 4(a)(1) threat categories.

Overutilization for Commercial, Recreational, Scientific, or 
Educational Purposes

    The primary threat to the narrownose smoothhound is overutilization 
in commercial and artisanal fisheries as the species is intensely 
fished throughout its entire range, including within its nursery 
grounds. In Argentina, M. schmitti is considered the most important 
elasmobranch in Argentine fisheries, making up 9-12 percent of the 
total landings from coastal fleets (Gal[iacute]ndez et al. 2010), and 
is the most heavily exploited shark species in artisanal fisheries. As 
bycatch in Argentine commercial bottom trawls, narrownose smoothhounds 
comprise around 20 percent of the coastal harvest from these fisheries 
(Colautti et al. 2010). In the 1990s, fishing for the species increased 
in the directed industrial shark fisheries (Massa et al. 2004a), with 
the narrownose smoothhound being the main shark caught in the Argentine 
Sea (based on an extracted biomass of 10,200 t for that time period), 
and the second most consumed domestic fish (Van der Molen et al. 1998; 
Chiaramonte 1998). Between 1981 and 1991, commercial catches of M. 
schmitti ranged from 5,000 t-8,000 t, with peak landings of 13,000 t in 
1988 (Cousseau and Perrotta 2000 cited in Massa et al. 2004a; FAO 
Global Capture Production Database). From 1992 to 1997, total catch of 
narrownose smoothhound remained fairly stable, hovering between 6,000 t 
and 8,000 t (Massa et al. 2004a), whereas the number of Argentine 
fishing vessels catching M. schmitti increased from 216 to 298 (Massa 
and Hozbor 2003). This increase in vessels and associated fishing 
pressure on the species consequently led to significant declines in the 
abundance of the species off the Argentine coast over this time period. 
Specifically, between 1992 and 1998, CPUE declined by 50 percent for 
the fishing fleet comprised of small-sized

[[Page 76087]]

vessels (<20 m) operating on the Argentine shelf, whereas the larger 
vessels (>20 m) that fished in deeper waters saw a decrease in CPUE of 
78 percent (Massa and Hozbor 2003). The larger fishing vessels also 
reported a decrease in the mean length of landed narrownose 
smoothhounds, from 59 cm in 1994 to 55 cm in 1999, a size smaller than 
estimated size at 50 percent maturity (Colautti et al. 2010). The 
decline in biomass and CPUE of the species, as well as the decrease in 
the average size of narrownose smoothhounds in the landings, all point 
to evidence of the significant historical overutilization of the 
species off the Argentine coast. In 2003, reported landings of 
narrownose smoothhound in Argentine ports reached 7,899 t, which 
exceeded the recommended maximum catch limit of 7,200 t for that year 
(Massa et al. 2004b), but between 2003 and 2007, mean values of CPUE of 
the species steadily increased, from 37.72 kg/h in 2003 to 42.3 kg/h in 
2007 (Perez et al. 2011). However, Perez et al. (2011) cautions that 
the increase in CPUE does not necessarily reflect an increase in 
abundance of the species. Rather the CPUE increase appears to be 
influenced by greater accessibility to the species (with the data 
indicating an increase in directed fishing effort for M. schmitti or a 
greater overlap of the species with other targeted species) (Perez et 
al. 2011).
    In the artisanal fisheries in Argentina, the narrownose smoothhound 
is a highly targeted shark, particularly in the coastal areas between 
36[deg] S. and 41[deg] S. latitudes. In Anegada Bay, a known nursery 
area for the shark, the smoothhound artisanal fishing season used to 
operate from October 15 to December 15, with fishermen exclusively 
using bottom gillnets to catch the sharks. In 2004, M. schmitti 
comprised 96 percent of artisanal landings from Anegada Bay; however, 
due to the selectivity of the artisanal gillnet sizes, only 1.8 percent 
of the fish captured were juveniles and 36.8 percent corresponded to 
pre-adults or young adults (Colautti et al. 2010). The catches ranged 
in size from 52-75 cm TL, which is generally below the recommended size 
for sustainable exploitation of this species (Cort[eacute]s 2007), 
although size at maturity in Anegada Bay has been estimated at 61 cm 
for males and 64 cm for females (Colautti et al. 2010). Since 2008, the 
smoothhound fishery in this bay has been closed as an additional level 
of protection for the species; however, Colautti et al. (2010) note 
that extensive coastal commercial fishing still occurs year-round in 
the surrounding El Rinc[oacute]n area in the southwest Buenos Aires 
province, which contains a number of nursery habitats for the species 
in addition to Anegada Bay. Because trawl nets are the predominant 
commercial gear used throughout the El Rinc[oacute]n area, a high 
proportion of the narrownose smoothhound catch in the coastal 
commercial fisheries are juveniles (Cousseau et al. 1998; Massa et al. 
2004a; Pereyra et al. 2008; Molina and Cazorla 2011). In addition, 
catches from this area comprise a significant proportion of the total 
Argentinian narrownose smoothhound landings, with El Rinc[oacute]n 
landings making up 37-53 percent of the national total of M. schmitti 
landings from 2003 to 2008 (Colautti et al. 2010). Colautti et al. 
(2010) suggests that this heavy coastal commercial fishing pressure on 
narrownose smoothhounds in the El Rinc[oacute]n area, especially in the 
nursery areas of the species, is not only leading to overfishing of the 
sharks in the region but is also contributing to a potential loss of 
genetic diversity, as individuals with the highest growth rate are 
preferentially removed from the population during fishing operations. 
Declines in the biomass of the species have already been reported from 
the El Rinc[oacute]n area, with estimates of up to 50 percent between 
1994 and 2003 (Colautti et al. 2010).
    In Uruguay, landings of smoothhounds (primarily M. schmitti, but 
also M. fasciatus and M. canis) increased dramatically between 1999 and 
2000, reaching 1,300 t, and then began to steadily decline, reaching 
approximately 850 t by 2005 (Domingo et al. 2008). According to data 
reported to the FAO, these estimates may be underestimated as the 
landings from Uruguay show peaks of 2,156 t and 3,212 t of narrownose 
smoothhound in 1998 and 1999, respectively (FAO Global Capture 
Production Database). True species composition of shark catches in 
Uruguay can be difficult because catch is often reported by common name 
and the same common name is used for multiple species (Nion 1999). 
However, similar to the Domingo et al. (2008) estimates, the FAO 
landings also decreased after 2001, with 892 t estimated in 2005. By 
2009, the narrownose smoothhound was considered overfished in the 
coastal regions of Uruguay (Defeo et al. 2009).
    In the AUCFZ, narrownose smoothhounds are the most heavily 
exploited shark (Segura and Milessi 2009). Though maximum permitted 
catch limits in the AUCFZ are set by both countries (Argentina and 
Uruguay), population declines have been seen throughout this portion of 
the narrownose smoothhound's range, mostly due to increased fishing 
effort on juveniles of the population (Colautti et al. 2010; Molina and 
Cazorla 2011). For example, samples taken in the port of Mar del Plata, 
where the largest percentage of the species is landed, indicate that in 
2001, nearly half of M. schmitti landings consisted of juveniles, with 
the average size of the landings estimated at 61.5 cm TL (Izzo and Rico 
2003 cited in Massa et al. 2004b). In 2002, the percentage of juveniles 
landed increased to 81.7 percent, and the average size of the 
narrownose smoothhound sharks in the landings decreased to 52.5 cm TL 
(Izzo and Rico 2004 cited in Massa et al. 2004b), a value below the 
size at maturity of the species (i.e., 55 to 60 cm TL). In other words, 
this level of utilization of the species, including the apparent 
removal of larger individuals from the population, led to a decrease in 
the average size of narrownose smoothhound sharks in landings, with the 
majority of the landings comprised of immature individuals. As litter 
sizes are correlated with maternal length, this removal of larger 
individuals from the population may significantly reduce the 
reproductive output of the species. Additionally, focusing fishing 
effort on primarily juveniles of the population can also have 
significant negative effects on recruitment (Vooren 1997) and may lead 
to further declines in the species. In fact, landings of the species in 
the AUFCZ have decreased in recent years, from 4,480 t in 2010 to 2,921 
t in 2014, a decline in catch of around 35 percent (CTMFM 2015). In 
addition, the estimated size at maturity of narrownose smoothhounds in 
the AUCFZ has chronologically decreased since the 1970s, which is also 
indicative of overutilization of the species in this area. 
Specifically, in 1978, the size at maturity for males and females was 
estimated to be 60 cm and 62 cm TL, respectively (Menni et al. 1986). 
In 1997, Diaz de Astarloa et al. (1997) calculated size of maturity 
using data from a 1993 winter coastal fishing cruise to be 54.9 and 
60.5 cm TL for males and females, respectively. Similarly, estimates 
calculated in 1998 determined the size at maturity to be 57.6 cm for 
males and 59.9 cm for females (Cousseau et al. 1998). More recently, 
Cort[eacute]s (2007) estimated the total size of maturity of the 
species to be 56.04 cm TL, which is lower than estimates in previous 
studies (Menni et al. 1986; Diaz de Astarloa et al. 1997; Cousseau et 
al. 1998) and is consistent with a declining population trend. Finally,

[[Page 76088]]

since 2008, total landings of M. schmitti reported by Argentina and 
Uruguay to the FAO have decreased by over 57 percent and 63 percent, 
respectively, although no corresponding effort information is 
available. Despite the multiple indicators of overutilization of the 
species, in 2013, Argentina landed a total of 4,379 t of M. schmitti 
and Uruguay landed 194 t (FAO Global Capture Production Database), 
suggesting the species is still considered valuable catch and bycatch 
in these countries.
    In Brazil, M. schmitti occurs as winter migrants on the Plataforma 
Sul off Rio Grande do Sul and, similar to R. horkelli and M. fasciatus, 
is caught by the trawl and oceanic gillnet fleets operating on the 
continental shelf. From 1975 to 1997, M. schmitti was one of two 
species that made up the majority of demersal shark landings in the 
port of Rio Grande (the other being the school shark, Galeorhinus 
galeus; Miranda and Vooren 2003). Targeted fishing for the species is 
thought to have increased from the mid 1970s through the 1980s, as 
evidenced by the near tripling of CPUE values of M. schmitti in the 
single trawl fleet, from 2.48 t/trip in 1975 to 7.31 t/trip in 1987 
(Miranda and Vooren 2003). Likewise, the CPUE of M. schmitti by pair 
trawls from 1975 to 1987 reflected a similar trend, increasing from 
0.35 t/trip to 2 t/trip (Miranda and Vooren 2003). However, CPUE values 
for both fleets decreased rapidly after 1987, with values in 1994 (1 t/
trip for single trawl and 0.3 t/trip for pair trawl) indicating an 
approximate 85 percent decline in abundance of M. schmitti from 1985 
numbers (Miranda and Vooren 2003). Despite the decline, M. schmitti was 
still being landed at the port of Rio Grande from April to October in 
1994 and 1995 by single trawl and oceanic gillnet fleets, with peak 
CPUE from these fleets corresponding with the seasonal occurrence of 
the species on the Plataforma Sul.
    Similar to the trends seen in the striped smoothhound within the 
coastal waters off southern Brazil, neonates of M. schmitti have also 
declined in abundance, a likely result of the intense coastal 
commercial and artisanal fishing along the Brazilian coast (see 
additional discussion of these fisheries in the assessments for 
Brazilian guitarfish and striped smoothhound). As mentioned previously, 
these coastal fisheries primarily use beach seines, gillnet and trawl 
gear in the nearshore locations off Rio Grande do Sul, habitat for 
narrownose smoothhound neonates and juveniles. Consequently, neonate M. 
schmitti populations that were once abundant in the 1980s have since 
seemingly disappeared, with data that show an absence of neonate 
individuals from artisanal beach net catches in 2003 and coastal trawl 
surveys conducted in 2005 (Vooren et al. 2005b). Further, Massa et al. 
(2006) report that a small local population of narrownose smoothhounds 
that was known to give birth in south Brazil in November and remain 
through February may have been extirpated, but additional information 
to confirm this potential extirpation is unavailable.
    As discussed in both the Brazilian guitarfish and striped 
smoothhound assessments, fishing by the industrial and artisanal fleets 
continues to occur at high efforts on the Plataforma Sul, and 
especially within the important coastal nursery and inner shelf 
habitats for the species (which overlap with both R. horkelli and M. 
fasciatus). This heavy fishing pressure may have led to the apparent 
extirpation of the local breeding population of narrownose smoothhound 
in southern Brazil (Massa et al. 2006 citing Vooren and Lam[oacute]naca 
unpublished data) and is likely contributing to the fishing mortality 
of the wintering migratory population. Based on the trends from 
available fisheries data (see R. horkelli and M. fasciatus 
assessments), it is unlikely that the industrial and artisanal fishing 
on the Plataforma Sul, and particularly off the coast of Rio Grande do 
Sul within narrownose smoothhound habitat, will decrease in the 
foreseeable future, indicating that overutilization (in the form of 
bycatch mortality) will continue to be a threat to the species leading 
to further declines in the wintering migratory population.

Inadequacy of Existing Regulatory Mechanisms

    In Argentina, there are few regulations in place to protect 
narrownose smoothhound nursery habitat. For example, R[iacute]a Deseado 
(~40 km; 47[deg]45' S.; 65[deg]55' W.), the southernmost limit of the 
narrownose smoothhound's range, is designated as a nature preserve and 
protects the local population from fishery-related mortality 
(Chiaramonte and Pettovello 2000). It has been identified as a nursery 
area, where breeding adults, neonates, and juveniles enter R[iacute]a 
Deseado waters in the late spring and stay until late summer 
(Chiaramonte and Pettovello 2000). Anegada Bay (39[deg]50'51'' S. to 
40[deg]43'08'' S. and 62[deg]28'44'' W. to 62[deg]03'00'' W.), 
Argentina, another known narrownose smoothhound nursery area, is also 
protected from fishing operations. The bay was previously designated as 
a multiple use zone reserve in 2000, which did little to protect the M. 
schmitti population from fishing mortality as a smoothhound fishery 
operated within the bay waters. However, in 2004 and 2008, fishing was 
banned in the bay due to concern over the conservation of the bay's 
natural resources, and since 2008, the smoothhound fishery in Anegada 
Bay has remained closed (Colautti et al. 2010). However, as Anegada Bay 
is surrounded by the larger El Rinc[oacute]n area, which also includes 
a number of other nursery habitats for the species and is open to 
fishing, it is unclear how effective the protections in Anegada Bay 
will be in decreasing the extinction risk of the species from 
overutilization. While these specific areas provide important 
protection for the species during critical life stages, they comprise a 
very small portion of the species' range and it is unclear to what 
extent the species relies on these small nursery areas for recruitment 
to the population.
    In Uruguay, regulations that likely contribute to decreasing the 
fishery-related mortality of the species include a summer trawling ban 
in 25 m to 50 m depths between La Paloma and Chuy and specific fishery 
area closures in the spring, summer, and autumn on the Uruguayan 
continental shelf, designated to protect juvenile hake (Merluccius 
hubbsi) but which also correspond with high use areas of the narrownose 
smoothhound population (Pereyra et al. 2008).
    Both Argentina and Uruguay list the narrownose smoothhound as a 
high priority species within their respective FAO NPOA-sharks (Domingo 
et al. 2008; Argentina FAO NPOA-sharks 2009). These plans, as stated 
previously, set goals to collect the necessary information on its 
priority species in order to conduct abundance assessments, increase 
research and improve management of the species, review current fishing 
licenses, and promote public awareness to release captured individuals. 
However, no updated results from the goals and priorities of these 
plans could be found. As such, the implementation and overall 
effectiveness of these plans at decreasing the threats to the 
narrownose smoothhound remains highly uncertain.
    In the AUCFZ, the area where current fisheries information 
indicates narrownose smoothhounds may likely be most abundant and 
heavily targeted, the Comisi[oacute]n T[eacute]cnica Mixta del Frente 
Mar[iacute]timo (CTMFM) is in charge of managing fish stocks and does 
so through the implementation of catch limits and fishery closures. For 
example, every year, the CTMFM implements a prohibition against

[[Page 76089]]

demersal trawling in an area that covers a large section of the common 
fishing zone, extending across the continental shelf, in order to 
protect vulnerable chondrichthyans from fishery-related mortality. This 
prohibition, which is usually in place between November and March, 
helps to decrease fishery-related mortality of the narrownose 
smoothhound shark during at least part of the year. The CTMFM also 
establishes additional area closures to trawling gear throughout the 
year in the AUCFZ, including within the Rio de la Plata (where 
historical estimates of narrownose smoothhound were as high as 44 t/
nm\2\; Cousseau et al. 1998), in order to protect whitemouth croaker 
(Micropogonias furnieri) and juvenile hake from overexploitation by the 
fisheries. As these areas correspond with high use by the narrownose 
smoothhound population, the trawling bans will also directly help to 
protect the narrownose smoothhound from additional fishery-related 
mortality.
    In terms of the direct management of M. schmitti sharks, from 2002 
to 2010, the CTMFM has set the total permissible catch limit for all 
Mustelus spp. at 4,850 t. In 2011, this limit was lowered to 4,000 t 
(Res. N[deg] 5/11, Res. N[deg] 5/02), and in 2012, the CTMFM set a 
species-specific total permissible catch limit for narrownose 
smoothhound at 4,500 t (Res. N[deg] 11/13, Res. N[deg] 9/12). This 
catch limit remained at this level until 2015, when it was reduced to 
3,500 t (Res N[deg] 6/15). However, despite these maximum allowable 
catch levels for Mustelus spp. that have been set since 2002, McCormack 
et al. (2007) reports that elasmobranch quotas and size regulations are 
largely ignored in Argentina and poorly enforced. This may explain why 
population declines continued to occur in this part of the species' 
range even after regulations were implemented to sustainably manage the 
species. Due to a lack of abundance data since 2003, it is unclear 
whether the catch limits for Mustelus spp. have positively affected the 
population since 2002, though it is worth noting that since 2010, 
catches of M. schmitti in the AUFCZ have been below the total allowable 
levels and on a decline (CTMFM 2015). However, perhaps the recent 
decline in M. schmitti landings prompted the reduction in catch limits 
in 2015.
    In Brazil, the narrownose smoothhound is listed on Annex 1 of 
Brazil's endangered species list and classified as critically 
endangered (Directive N[deg] 445). As described in previous species 
assessments, an Annex 1 listing prohibits the catch of the species 
except for scientific purposes, which requires a special license from 
IBAMA. There is also a prohibition of trawl fishing within three 
nautical miles from the coast of southern Brazil, although the 
enforcement of this prohibition has been noted as difficult 
(Chiaramonte and Vooren 2007). In addition, the species is still 
susceptible to being caught as bycatch in the legally permitted coastal 
gillnet fisheries and offshore trawl and gillnet fisheries and 
vulnerable to the associated bycatch mortality (Lessa and Vooren 2007). 
Additionally, unlike the striped smoothhound, the narrownose 
smoothhound is listed as one of the 12 species of concern under 
Brazil's FAO NPOA-sharks and would also benefit from the proposed 
fishing closures and other management measures outlined in the plan. 
However, as mentioned previously, the plan was only just approved as of 
December 2014, and will not be fully implemented for another 5 years. 
Thus, the implementation and effectiveness of the recommendations 
outlined in the plan remain uncertain, with the best available 
information indicating that current regulatory measures in Brazil to 
protect vulnerable species are poorly enforced.

Extinction Risk

    The best available information provides multiple lines of evidence 
indicating that the M. schmitti currently faces a moderate risk of 
extinction. Below, we present the demographic risk analysis, threats 
assessment, and overall risk of extinction for the narrownose 
smoothhound shark.

Demographic Risk Analysis

Abundance
    There is limited information available regarding quantitative 
abundance estimates of narrownose smoothhound throughout its range. 
However, biomass estimates as well as trends in commercial landings and 
CPUE data can provide some insight into the abundance of the species. 
The narrownose smoothhound is the most abundant and widely distributed 
triakid in the Argentine Sea. In Argentina, the narrownose smoothhound 
is mainly landed by the commercial fleet operating in the Buenos Aires 
coastal region, and represents up to 14.5 percent of landings (Carozza 
et al. 2001 cited in Massa et al. 2004b). Between 1992 and 1997, 
landings of the species in Argentina were fairly stable, on the order 
of 6,000-8,000 t; however, CPUE values decreased by upwards of 78 
percent during this time period, indicating a likely decline in the 
abundance of the species. From 1998 to 2002, biomass of M. schmitti 
reportedly declined in the main fishing areas along the coast of Buenos 
Aires Province and the surrounding region by approximately 22 percent 
(Massa et al. 2006). National landings also decreased in Argentina by 
30 percent during this same time period and have continued to decline 
based on FAO landings data through 2013. It is important to note that 
the decrease in landings is not due to falling market values as M. 
schmitti continues to fetch a high price in the Argentine domestic 
market (Massa et al. 2004b). In 2003, the spring time abundance of M. 
schmitti from coastal Buenos Aires and Uruguay (between 34[deg] S.-
41[deg] S.) was estimated to be 88,500 t, which represents a 50 percent 
and 39 percent decline from estimated values in 1994 and 1999, 
respectively (Massa et al. 2004a). Additionally, based on estimates 
calculated in 2007, size at maturity of the species has chronologically 
decreased since the 1970s, a strong indication of overutilization of 
the species and declining abundance.
    In Uruguay, there is conflicting information regarding the trend in 
catches of M. schmitti. Landings of smoothhounds in Uruguay are 
aggregated at the genus level because catch is often reported by common 
name and the same common name is used for multiple species. Thus, 
identifying the true species composition of shark catches in Uruguay is 
problematic. According to Domingo et al. (2008), landings of 
smoothhounds in Uruguay (primarily M. schmitti) increased dramatically 
between 1999 and 2000, reaching 1,300 tons, and then steadily declined 
to approximately 850 tons by 2005. Based on landings data reported to 
the FAO, catches of M. schmitti have continued to decline, with only 
194 t reported in 2013. However, without corresponding effort 
information, it is unclear if the decrease in landings is a result of 
decreases in abundance in the species.
    In Brazil, M. schmitti occurs as winter migrants on the Plataforma 
Sul and is caught by the trawl and oceanic gillnet fleets operating on 
the continental shelf. Based on CPUE data from these fleets, the 
wintering population has likely suffered significant declines in 
abundance. The CPUE values from both the single and pair trawl 
fisheries showed an increase from the mid 1970s to the late 1980s; 
however, after 1987, CPUE values for both fleets decreased rapidly, and 
in 1994, these CPUE values showed an approximate 85 percent abundance 
decline of M. schmitti from 1985 values (Miranda and Vooren 2003). 
Massa et al. (2006) also cites

[[Page 76090]]

unpublished data that indicate the likely extirpation of a local 
breeding population of narrownose smoothhound in Brazil as a result of 
fishing in inshore pupping and nursery areas. Although no further 
information was given regarding this population, survey and fisheries 
data suggest significant declines in newborn M. schmitti from a local 
nursery area off the coast of Rio Grande do Sul. Once abundant in the 
1980s in the coastal waters off Casino Beach, Rio Grande do Sul, 
neonates of this local population have since seemingly disappeared, 
with data that show an absence of individuals from artisanal beach nets 
in 2003 and coastal trawl surveys in 2005 (Vooren et al. 2005b). This 
absence of neonates, compared to data from the 1980s, is likely a sign 
of decline of this population and may even suggest a potential 
extirpation.
    Overall, best available information suggests the species is likely 
in decline in parts of its Argentine and Uruguayan range, and has 
experienced a significant decrease in abundance in its winter migrant 
population in Brazil. Although present abundance estimates are unknown, 
the significant declines in both CPUE and landings of the species 
throughout its range, as well as the chronological reduction of the 
species' average size (based on landings data) and size of maturity, 
suggest overexploitation of the species and a declining abundance 
trend. Targeting of the species will continue, given its demand in the 
market and importance in both the artisanal and commercial fisheries in 
the region and, combined with the high fishing pressure in the species' 
nursery areas, the species may continue to experience population 
declines throughout its range, with abundance levels that will likely 
contribute significantly to its extinction risk in the foreseeable 
future.
Growth Rate/Productivity
    The narrownose smoothhound has an estimated lifespan of 20.8 years 
and 24.7 years for males and females, respectively, with a maximum 
recorded size of 110 cm TL. Information regarding size and age of 
maturity estimates vary throughout the species' range, but the most 
recent estimate from Hozbor et al. (2010) suggests an age at maturity 
of 4 years for both sexes. Although M. schmitti has an annual 
reproductive cycle with a lengthy gestation period (11 months) and an 
average of only 4-5 pups per litter, the species' intrinsic rate of 
population increase is relatively high, at 0.175 per year. Natural 
mortality rates ranged from 0.139 to 0.412 (Cort[eacute]s 2007). These 
estimates indicate that M. schmitti has a higher potential to recover 
from exploitation compared to other coastal sharks, and could withstand 
annual removal rates of up to approximately 10 percent of the 
population. However, based on confirmed chronological reductions in 
both average size (from landings data) and total length at maturity in 
the species, it is apparent that removal rates of the species have been 
exceeding the 10 percent sustainable removal rate. The reduction in 
mean size and size at maturity is particularly concerning due to the 
positive relationship between maternal length and litter size (i.e., 
litter size increases significantly with maternal length) in which a 
decrease in maximum size has the potential to reduce the species' 
reproductive output. As such, these reductions likely compromise the 
species' growth rate and productivity, and consequently, hinder its 
ability to recover from exploitation.
Spatial Structure/Connectivity
    Very limited information is available regarding spatial structure 
and connectivity of M. schmitti populations. Tagging studies of related 
species M. antarcticus and M. lenticulatis found that they have high 
dispersal capacities (Francis 1988), but no such studies have been 
conducted specifically for M. schmitti. If narrownose smoothhound 
populations are connected, then the significant fishing pressure on the 
migratory population while they winter on the Plataforma Sul may be 
negatively impacting the populations found in other parts of the 
species' range (perhaps contributing to the observed declines off 
Argentina and Uruguay). However, based on the available data, there is 
not enough information to identify critical populations or determine 
whether the rates of dispersal among populations, metapopulations, or 
habitat patches are posing a risk of extinction.
Diversity
    The loss of diversity can increase a species' extinction risk 
through decreasing a species' capability of responding to episodic or 
changing environmental conditions. This can occur through a significant 
change or loss of variation in life history characteristics (such as 
reproductive fitness and fecundity), morphology, behavior, or other 
genetic characteristics. In terms of population structure, only one 
genetics study has been conducted to determine if multiple stocks occur 
throughout the species' range (Pereya et al. 2010). Results of this 
study indicate that M. schmitti comprises a single demographic unit in 
the R[iacute]o de la Plata area and its maritime front (area separating 
Uruguay and Argentina), with no distinct population structure found 
between or within the R[iacute]o de la Plata, the Atlantic coast or its 
outer shelf. These findings indicate high connectivity and suggest 
genetic homogeneity over this geographic range, which is attributed to 
the likely high dispersal and migration rates of the species (Pereya et 
al. 2010). However, a lack of genetic structure can also result from 
many other factors, including large effective population sizes and/or 
the presence of shared ancestral polymorphisms due to recent population 
divergence.
    In addition to genetic homogeneity, the study found that nucleotide 
diversity in M. schmitti was lower than that reported for other 
elasmobranchs. These results may indicate that narrownose smoothhound 
experienced a genetic bottleneck, recent expansion, or selection, which 
potentially occurred during the Pleistocene Era (Pereyra et al. 2010). 
However, it is difficult to unambiguously discern between evidence for 
natural selection and demographic population expansion. Overall, the 
low genetic diversity values found for the species and evidence that 
fishing pressure may have already altered the genetic characteristics 
of the population (i.e., smaller average size and size at maturity, 
which in turn can alter reproductive fitness and fecundity) raise 
considerable concern over the species' status. This information 
indicates that M. schmtti may be at an increased risk of inbreeding 
depression or random genetic drift, and could experience the fixing of 
recessive detrimental genes, reducing the overall fitness of the 
species.

Threats Assessment

    The primary threat to narrownose smoothhounds is overutilization in 
commercial and artisanal fisheries, with the species both targeted and 
bycaught throughout its range. In Argentina, M. schmitti is considered 
the most important elasmobranch for Argentine fisheries; however, data 
suggest that the majority of narrownose smoothhounds caught by 
Argentine fishermen are juveniles (e.g. up to 81.7 percent of the 
landings in 2002), indicating significant fishing pressure in important 
nursery areas. Declines in both CPUE and biomass of M. schmitti in 
Argentina occurred throughout the 1990s and early 2000s; however, mean 
values of CPUE have shown a slight upward trend from 2003-2007. 
However, as noted previously, these values should be interpreted with 
caution as they could

[[Page 76091]]

be the result of increased directed fishing pressure on M. schmitti or 
an increase in overlap of fishing vessels in areas where M. schmitti 
has higher concentrations. Further, the chronological reduction in mean 
size and size of sexual maturity since the 1970s indicates overfishing 
of the species, suggesting exploitation rates are higher than what the 
species can presently sustain.
    In the AUCFZ, where M. schmitti is most heavily exploited, fishing 
regulations currently set total permissible catch of M. schmitti at 
3,500 t (which is a reduction from the 4,500 t limit that was in place 
since 2012). Additionally, trawling is banned within 5 nm of the coast, 
which coincides with the pupping and breeding areas of the species. 
While there is no information to indicate whether these regulatory 
mechanisms are positively affecting the status of the narrownose 
smoothhound, particularly since species-specific catch limits for M. 
schmitti have only been implemented since 2012, these regulations may 
help reduce fishing pressure in this important part of the species' 
range. Since 2010, catches of M. schmitti in the AUFCZ have been below 
the total allowable levels (for Mustelus spp. and M. schmitti) and on a 
decline; however, it should be noted that despite total allowable 
catch, minimum sizes, and annual quotas in place for many elasmobranchs 
in Argentina, they are largely ignored and poorly enforced (McCormack 
et al. 2007).
    In Uruguay, narrownose smoothhounds are both targeted in artisanal 
fisheries and caught as bycatch. Despite the difficulties in 
identifying species composition of shark catches and discrepancies in 
catch information, data indicate landings of M. schmitti have declined 
in Uruguay, and in 2009, the species was classified as overfished in 
coastal regions of Uruguay and considered a high priority under the 
country's FAO NPOA-sharks.
    In southern Brazil, the intensive fishing effort on the Plataforma 
Sul has likely led to overutilization, and consequently, significant 
declines in the winter migrant population of M. schmitti and potential 
extirpation of a local breeding population. Bottom trawl fishery CPUE 
data provide evidence that abundance of the winter migrant population 
of M. schmitti decreased by 85 percent due to intensive fishing effort 
from 1985 onwards. The absence of neonates from coastal waters, where 
they were once abundant in the 1980s, also suggest that intense fishing 
effort, especially in important nursery areas, has led to significant 
declines in local populations and potential extirpation of a small 
population of Brazilian migrants that was known to give birth in south 
Brazil in November and remain through February (Massa et al. 2006). 
Since 2004, the species has been listed on Brazil's endangered species 
list, which prohibits fishers from catching this species. The species 
is also listed as one of 12 species of concern under Brazil's FAO NPOA-
sharks, which calls for fishing closures in areas of <20 m deep that 
would provide protection to neonates and juveniles, as well as other 
closures to protect adult aggregations; however, the implementation and 
effectiveness of the recommendations outlined in the plan remain 
uncertain, with the best available information indicating that current 
regulatory measures in Brazil to protect vulnerable species are poorly 
enforced, particularly in artisanal fisheries.
    Based on the best available information, it is evident that M. 
schmitti is heavily exploited and has likely experienced population 
declines throughout its range as a result of historical and continued 
overutilization of the species. In limited parts of the species' range, 
regulatory mechanisms are seemingly adequate to control for 
overutilization, such as the closures of important nursery areas in 
Argentina which protect neonates and juveniles from fishing mortality. 
However, throughout large portions of the species' range, particularly 
in areas where the species is most heavily exploited, it is evident 
that regulatory mechanisms are not adequately protecting the species 
from further decline. For example, in the AUCFZ, continued population 
declines have been seen in this part of the species' range through 2005 
(Massa and Hozbor 2008), despite annual maximum allowable catches for 
Mustelus spp. since 2002. Additionally, while CPUE values in Argentina 
have shown a slight upward trend from 2003-2007, the cause of this 
trend is uncertain and may actually reflect increased direct and 
indirect fishing effort on M. schmitti. While species-specific catch 
limits were implemented for M. schmitti in 2012, it is unclear if these 
levels are adequate to prevent further declines in the species. 
Although corresponding effort data are unavailable, since 2008, 
landings of M. schmitti reported by Argentina and Uruguay to the FAO 
have decreased by over 50 percent. Since 2010, catches in the AUFCZ 
have been below the total allowable catch levels and also on a decline, 
which may suggest reducing fishing pressure on the species or evidence 
that catch regulations are potentially being followed. However, 
McCormack et al. (2007) note that quotas and size regulations are 
largely ignored and lack enforcement in Argentina. Additionally, since 
2006, the total number of vessels in Argentina's fishing fleet has 
remained fairly stable (OECD 2014), potentially indicating that fishing 
effort has not decreased substantially in recent years. As such, the 
decreasing landings, even below total allowable catch limits, may 
indicate a continued decline in the abundance of the species. Overall, 
based on the best available information, we find that existing 
regulatory measures throughout the most heavily exploited areas of the 
species' range are inadequate to protect the species from 
overutilization, which is the main threat significantly contributing to 
the extinction risk of M. schmitti.

Risk of Extinction

    While there is considerable uncertainty regarding the species' 
current abundance, the best available information indicates that the 
species has experienced population declines of significant magnitude 
throughout its range. Most concerning is the evidence to suggest M. 
schmitti has undergone a chronological decline in average size (based 
on landings data) and mean size of maturity, as shown in studies from 
the 1970s through 2007 (Massa et al. 2004a; Cort[eacute]s 2007). Not 
surprisingly, this decreasing trend corresponds to an increase of 
fishing operations and provides evidence of the negative impact of 
historical and current exploitation rates and associated fishing 
mortality on the biological status of the species. Because of the 
positive relationship between maternal length and litter size for the 
species, a decrease in the average size of the population has the 
potential to reduce the species' reproductive output. Furthermore, a 
decrease in average size below the species' mean size of maturity can 
hasten the reduction of biomass and increase the risk of local 
extinction (Baum and Myers 2004 cited in Massa et al. 2004b). Although 
the species' relatively high intrinsic rate of population increase and 
ability to withstand moderate levels of exploitation up to 10 percent 
of the total population provides the narrownose smoothhound shark with 
some protection from extinction, and is likely the reason why the 
species remains the most abundant houndshark in the Argentine Sea, the 
aforementioned decreases in average size and size at maturity as well 
as population size suggest the species is being exploited at a level 
exceeding what it can sustain. Thus, based on the best available

[[Page 76092]]

information, we conclude that the species is currently at a moderate 
risk of extinction due to declining trends in abundance and population 
growth/productivity, which are unlikely to reverse in the foreseeable 
future because of the continued overutilization of the species in 
commercial and artisanal fisheries and inadequacy of existing 
regulatory measures to control this level of exploitation.

Protective Efforts

    With the exception of the recommendations within the FAO NPOA-
sharks discussed above, we were unable to find any other information on 
protective efforts for the conservation of narrownose smoothhound in 
Argentina, Uruguay, or Brazil that would potentially alter the 
extinction risk for the species. We seek additional information on 
other conservation efforts in our public comment process (see below).

Proposed Determination

    Based on the best available scientific and commercial information 
as presented in the status review report and this finding, we find that 
the narrownose smoothhound is not presently in danger of extinction 
throughout its range, but likely to become so in the foreseeable 
future. We assessed the ESA section 4(a)(1) factors and conclude that 
the species faces ongoing threats from overutilization and inadequacy 
of existing regulatory mechanisms throughout its range. Due to the 
species' relatively fast population growth rate (for elasmobranchs) and 
likely high historical abundance, it can withstand moderate rates of 
exploitation. However, based on the declining trends in the species' 
abundance, its low genetic diversity, the observed decreases in average 
size of the species in catches as well as the decreases in size at 
maturity in areas where it is most heavily exploited, best available 
data suggest that the fishing mortality rate is higher than what the 
species can sustain. Although the species' present level of abundance 
does not appear to be at such a low level to trigger the onset of 
depensatory processes, the species' observed downward trend is unlikely 
to reverse in the foreseeable future as a result of continued 
overutilization. We therefore conclude that the species is on a 
trajectory indicating that it will more likely than not be at risk of 
extinction in the foreseeable future. We also found no evidence of 
protective efforts for the conservation of narrownose smoothhound that 
would reduce the level of extinction risk faced by the species. We 
therefore propose to list the narrownose smoothhound as a threatened 
species.

Angel Sharks

    Angel sharks are members of the family Squatinidae. Both the spiny 
angel shark (Squatina guggenheim) and Argentine angel shark (Squatina 
argentina), two of the elasmobranchs considered for listing in this 
finding, can be found in the Southwestern Atlantic Ocean from southern 
Brazil to Argentina. The taxonomy of angel sharks of the southwestern 
Atlantic Ocean has been a source of ongoing controversy (Vooren and 
Chiaramonte 2006). Due to similar morphological characteristics, S. 
argentina, S. guggenheim, S. occulta, and S. punctata have been 
variously synonymized with each other (Compagno 2005; Vooren and 
Chiaramonte 2006; de Carvalho 2012). Currently, S. punctata is 
considered a junior synonym of S. guggenheim (Vooren and da Silva 1991; 
de Carvalho et al. 2012; Vaz and Carvalho 2013). Extensive studies of 
the morphotypes that occur in southern Brazil and the southwestern 
Atlantic concluded that S. argentina, S. guggenheim, and S. occulta are 
three different species that can be distinguished by morphological 
differences as well as life history characteristics, such as 
differences in reproductive patterns, overall size, and depth and 
temperature preference (Vooren and da Silva 1991; Vaz and Carvalho 
2013). An analysis of molecular systematics of angel sharks confirms 
the validity of S. guggenheim and S. occulta as separate species 
(Stelbrink et al. 2010).

Spiny Angel Shark (Squatina guggenheim)

Species Description

    The spiny angel shark (S. guggenheim) can be distinguished from its 
sympatric species by the presence of a median row of spines or 
tubercles on its dorsal side (Vooren and da Silva 1991; Milessi et al. 
2001; Sch[auml]fer et al. 2012; Vaz and Carvalho 2013). There are 30-35 
spines, which are short, conical, and slightly recurved, between the 
head and the first dorsal fin. As females mature, their dorsal spines 
become less distinct and take the form of flattened tubercles, whereas 
juveniles less than 35 cm TL of both sexes have spines flanked on each 
side by a diffuse row of smaller spines (Vooren and da Silva 1991). 
Adult males have small spines on the outermost tips of the dorsal 
surface of their pectoral fins that are inclined towards the shark's 
midline. The outer edges of the pectoral fins are straight and the 
posterior corners are located nearer to the origin of the pelvic fin 
than to the outer corner of the pelvic fins (Vooren and da Silva 1991). 
The dorsal skin is light to dark brown with several white or creamy-
white to yellowish large, rounded blotches that are variable in size 
and symmetrically distributed on the entire dorsal surface (Vaz and 
Carvalho 2013).

Range and Habitat Use

    The spiny angel shark is found in the southwestern Atlantic Ocean 
from Esp[iacute]rito Santo, Brazil, to Rawson, Argentina (Milessi et 
al. 2001; V[ouml]gler et al. 2003; Awruch et al. 2008). It is a 
primarily coastal, bottom dwelling angel shark (Chiaramonte and Vooren 
2007; Crespi-Abril 2013). Spiny angel sharks prefer depths between 10 m 
and 80 m, but have been reported as deep as 150 m off Argentina 
(Cousseau 1973; Chiaramonte and Vooren 2007), and occur in temperatures 
between 10 [deg]C and 22 [deg]C (Vooren and da Silva 1991). The species 
lives in muddy or sandy bottom substrates and is relatively inactive 
during the day. This nocturnal activity makes the spiny angel shark 
more vulnerable to gillnet fisheries, which tend to operate at night 
(Vooren and Klippel 2005a).

Diet and Feeding

    Spiny angel sharks are thought to be sit-and-wait predators, lying 
motionless on the bottom until prey passes closely overhead. The prey 
is then grasped by an upward bite (Vooren and da Silva 1991). Based on 
diet studies, the spiny angel shark appears to prefer bony fishes but 
will also feed on crustaceans, molluscs, and polychaetes (V[ouml]gler 
et al. 2003; Colonello 2005; V[ouml]gler et al. 2009). In the AUCFZ, a 
study of spiny angel shark trophic ecology found that, numerically, 
bony fish made up the vast majority of the diet, at 89.7 percent 
(V[ouml]gler et al. 2003). Crustaceans (4.8 percent), molluscs (4.4 
percent), and polychaetes (0.46 percent) made up the remaining portions 
(V[ouml]gler et al. 2003). Spiny angel sharks consumed both pelagic and 
demersal fishes including Engraulis anchoita, Cynoscion guatucupa, 
Patagonotothen ramsayi, Notothenia longipes, and Merluccius hubbsi. The 
crustaceans consumed were primarily shrimps (Penaeidae), while the 
squid Illex argentinus was the only species of mollusc consumed 
(V[ouml]gler et al. 2003, 2009).
    Although ontogenetic and seasonal differences in diet have been 
observed for the species (V[ouml]gler et al. 2003; Colonello 2005; 
V[ouml]gler et al. 2009), bony fish remain the primary prey item for 
all size classes and during all

[[Page 76093]]

seasons, and, generally, as size of the spiny angel shark increases so 
does its trophic level. Ranging from a minimum trophic level of 3.69 
for the smallest length group of spiny angel shark (23-60 cm) to a 
maximum trophic level of 4.40 for the largest length group (81-91 cm), 
the entire population of spiny angel sharks in the AUFCZ was estimated 
to have a trophic level of 3.90 (V[ouml]gler et al. 2003; 2009). For 
comparison, in aquatic environments, trophic levels tend to range from 
2 (for species that are lower on the food chain, such as herbivores and 
detritivores) to 5.5 (for predators of marine mammals, such as the 
polar bear and killer whale) (Pauly et al. 2014).

Growth and Reproduction

    Very few age and growth studies on the spiny angel shark could be 
found. In terms of length frequency distributions of spiny angel 
sharks, individuals caught in the San Mat[iacute]as Gulf, Argentina 
showed a modal peak of 75-90 cm TL for males and 80-95 cm TL for 
females, with no evidence of size dimorphism (Awruch et al. 2008). The 
largest recorded animals were 95 cm TL for both sexes (Awruch et al. 
2008). Length at 50 percent maturity for males was reached at 76 cm TL 
and for females at 73 cm TL (Awruch et al. 2008).
    Studies of spiny angel sharks farther north, in Rio de la Plata and 
El Rinc[oacute]n, Argentina, found that males from El Rinc[oacute]n at 
a given length were significantly heavier than males from Rio de la 
Plata, while females showed no significant differences in the length-
weight relationship (Colonello et al. 2007). Both sexes grew larger in 
El Rinc[oacute]n than in Rio de la Plata (Colonello et al. 2007); but, 
length at 50 percent maturity in males was not significantly different 
between El Rinc[oacute]n and Rio de la Plata (75 cm TL and 72.45 cm TL, 
respectively). However, length at 50 percent maturity was significantly 
different between study areas for females, with estimates of 71.34 cm 
TL in Rio de la Plata and 77.01 cm TL in El Rinc[oacute]n (Colonello et 
al. 2007).
    In southern Brazil, spiny angel sharks reach a maximum length of 92 
cm TL and age of 12 years (Vooren and Klippel 2005a). According to the 
characteristics for the S. guggenheim population presented in Vooren 
and Klippel (2005a), the relative growth rate (k) of the species from 
the von Bertalanffy growth equation is 0.275 year-\1\ with a 
theoretical maximum size (L[infin]) of 94.7 cm TL. Length 
and age at first maturity is estimated to be 72 cm TL and 4 years, 
respectively (Vooren and Klippel 2005a).
    In terms of reproduction, the spiny angel shark has only one 
functional ovary (Vooren and da Silva 1991), with the maturation of 
ovarian follicles lasting about 2 years before ovulation, followed by 
gestation (Colonello et al. 2007). The female reproductive cycle is 
thought to be triennial (Colonello et al. 2007), with a gestation 
period that likely lasts 12 months (Colonello et al. 2007). Gestation 
begins in the summer (January-February) and pupping occurs the 
following spring (November-December) (Sunye and Vooren 1997). Gestation 
is divided into two stages: Uterine gestation and cloacal gestation. 
Early gestation (January-April) occurs only in the uteri, which 
contains recently ovulated eggs and embryos up to 25 mm TL (Sunye and 
Vooren 1997). During mid-term gestation and parturition (June-November) 
the uteri undergo a physical reconfiguration, causing the uteri and 
cloaca to form a heart-shaped chamber where the embryos develop (Sunye 
and Vooren 1997). According to Sunye and Vooren (1997), because this 
uterine-cloacal chamber is open to the external environment through a 
cloacal vent, this anatomical configuration is thought to be the reason 
why Squatina species are observed easily aborting embryos during 
capture or handling.
    Pupping occurs during the spring and summer months (September-
March) in depths less than 20 m (Vooren 1997; Miranda and Vooren 2003). 
Litter sizes for the species range between 2 and 8 pups (Colonello et 
al. 2007; Vooren and Klippel 2005a). For spiny angel sharks in 
Argentina, Colonello et al. (2007) estimated an average of 4.07 pups 
per litter, with fecundity increasing with female length. In contrast, 
Vooren and Klippel (2005a) note that spiny angel sharks in southern 
Brazil frequently have 5 or 6 pups per litter, with the number of pups 
unrelated to female length. However, given the 3-year reproductive 
cycle, the range in pup estimates for spiny angel sharks results in a 
very low annual fecundity for the species (e.g., between 0.67 and 2.67 
pups per year) (Colonello et al. 2007; Vooren and Klippel 2005a). After 
pupping, juveniles of the species will remain in the shallow waters for 
one year before migrating out to the continental shelf (Vooren and da 
Silva 1991; Vooren 1997; Vooren and Klippel 2005a). In terms of known 
juvenile habitat, the area of Rio Grande do Sul between 31[deg]50' S. 
and 33[deg]30' S. at depths less than 20 m is considered a nursery area 
for spiny angel sharks (Vooren and Klippel 2005a).

Genetics and Population Structure

    Recently, Garcia et al. (2015) examined the population structure of 
the spiny angel shark in the middle of its range, in and around the Rio 
de la Plata estuary. Using mitochondrial DNA (which is maternally-
inherited DNA), the authors found that individuals from the outer 
estuary, surrounding coastal sites, and the outer shelf of the 
southwestern Atlantic showed no evidence of population genetic 
structuring. However, examination of nuclear recombinant DNA genes 
(which are biparentally-inherited) indicated that there was a 
remarkably high level of population genetic structure between the outer 
shelf spiny angel sharks and the coastal and outer estuarine angel 
sharks. In other words, the samples of spiny angel shark from the outer 
shelf represent an isolated group from the samples of spiny angel shark 
from the coastal and outer estuarine sites. Additionally, mitochondrial 
DNA indicated that the number of immigrant females per generation from 
the outer shelf to the Atlantic coast was much lower (2.8 individuals 
per generation) than the number of immigrant females per generation 
between the other populations (with estimates ranging from 12.8-46.9 
individuals). All analyses revealed very low values of haplotype and 
nucleotide diversity from the recombinant DNA genes. Based on the low 
level of genetic diversity detected in S. guggenheim, Garcia et al. 
(2015) suggest the species has either undergone a long-term population 
decline or experienced a population bottleneck and recent expansion. 
Either scenario suggests a vulnerability to overexploitation, given the 
species' longevity and low reproductive potential. However, additional 
genetic studies are needed to better understand these patterns (Garcia 
et al. 2015).

Demography

    Information on natural mortality rates or the intrinsic rate of 
population increase of the spiny angel shark is currently unavailable.

Historical and Current Distribution and Population Abundance

    In northern Argentina, spiny angel sharks are considered to be a 
eurythermic coastal shelf species with highest abundances on the outer 
coastal shelf between depths of 28.9 m and 49.6 m (Jaureguizar et al. 
2006). In the Rio de la Plata estuary, Argentina, spiny angel sharks 
were present most frequently in the deepest estuarine zone (12.6 m-16 
m) with salinities between 25 and 34 psu. They are not considered a

[[Page 76094]]

permanent resident of the estuary, with abundances higher in the summer 
than during the spring and fall (Jaureguizar et al. 2003).
    In the AUCFZ, spiny angel shark distribution appears to be 
influenced by temperature, with clear avoidance of water temperatures 
below 5 [deg]C and above 20 [deg]C (V[ouml]gler et al. 2008). 
Specifically, V[ouml]gler et al. (2008) found that spiny angel sharks 
concentrate in water temperatures between 13.2 [deg]C and 18.5 [deg]C 
in the spring and between 7.0 [deg]C and 15.0 [deg]C in the fall. They 
prefer salinities between 33.4 and 33.5, with avoidance of salinities 
below 33.0 and above 34.0. Additionally, a strong association was found 
between spiny angel shark presence and thermal horizontal fronts, which 
indicates that temperature is the principal environmental variable that 
influences distribution (V[ouml]gler et al. 2008). In Rio de la Plata, 
in the AUCFZ, spiny angel shark densities are particularly high along 
the Uruguayan coast in the spring, which is thought to be related to 
the presence of higher salinity waters on the Uruguayan coast than the 
Argentine coast during this season (Colonello et al. 2007).
    In southern Brazil, spiny angel sharks are considered a resident 
species (Vooren 1997). From 1980-1984 spiny angel sharks were common 
year round on the southern shelf (at depths between 10 m and 100 m) 
from Solid[atilde]o to Chu[iacute], with some areas recording CPUE 
densities as high as 50 kg/h (Vooren and Klippel 2005a). According to 
Vooren and Klippel (2005a), a portion of the S. guggenheim population 
makes seasonal migrations across the continental shelf, which is 
related to the 3-year reproductive cycle of the species (i.e., one 
third of adult females in the population will migrate per year to give 
birth). Specifically, this inshore migration is into depths between 10 
m and 40 m and occurs in the spring and summer (September-March) for 
pupping and likely mating purposes (as adults of both sexes conduct 
this migration in addition to pregnant females) (Vooren 1997; Miranda 
and Vooren 2003). As mentioned previously, newborns remain in these 
shallow waters (<20 m) for the first year of their life before 
migrating to deeper waters on the continental shelf. The other, larger 
portion of the population, which is not moving seasonally and includes 
both juveniles and adults of both sexes, are most abundant in depths of 
40 m to 60 m year-round (Vooren and Klippel 2005a). In fact, research 
surveys off of Ubatuba, S[atilde]o Paulo, Brazil caught spiny angel 
sharks in shallow sampling stations around 20 m deep, but found that 
they were most abundant near 50 m depths (Rocha et al. 1998).
    In general, very few abundance estimates are available for the 
species. According to Chiaramonte and Vooren (2007), the spiny angel 
shark is likely composed of smaller, localized populations throughout 
its range. In Argentinian waters, fishery surveys and commercial data 
provide limited indication of abundance and trends in this part of the 
species' range. In 1993, for example, the abundance of spiny angel 
sharks in the San Mat[iacute]as Gulf, Argentina (southern Argentina) 
was estimated to be 192.53 t (Argentina FAO NPOA-sharks 2009); however, 
the San Mat[iacute]as Gulf makes up a very small portion (approximately 
9.6 percent) of the spiny angel shark's range and no recent abundance 
estimates could be found. Surveys of the continental shelf in northern 
Argentina (between 34[deg] S. and 41[deg] S.; approximately 20 percent 
of the species' range), conducted during the spring when abundance of 
spiny angel sharks is highest, provided estimates of mean biomass 
density of 0.518 t/nm\2\ in 1981, 1.305 t/nm\2\ in 1995, and 0.394 t/
nm\2\ in 1999 (Jaureguizar et al. 2006). Catch rates of the species 
were also fairly high based on data from trawl research surveys 
conducted in this same area from October 1997 to June 1998, especially 
during the inshore spring/summer migration months (September to March). 
Specifically, CPUE ranged from 25 sharks/30 min of trawling in March to 
80 sharks/30 min of trawling in October (Vogler et al. 2008). A later 
study, conducted from 2000-2003 and in the same area, also recorded 
high densities of the species during the spring months (November-
December) with estimates of 750 to <1500 kg/km\2\ (equivalent to 2.58-
5.15 t/nm\2\) (Colonello et al. 2007). However, based on fishery-
independent data collected during research surveys conducted in the 
winter of 1993 and 2004, and spring of 1994, 1999, 2003, and 2005, 
Massa and Hozbor (2008) observed a decrease in the biomass of S. 
guggenheim, mainly between the winter seasons of 1993 and 2004. Trends 
in biomass for the spring time cruises were less clear, with decreases 
estimated between 1994 and 1999 and between 2003 and 2005, and 
increases between 1999 and 2003 (Massa and Hozbor 2008). Declines were 
also observed in the CPUE of fishing fleets operating on the 
Argentinian shelf, particularly for the smaller-sized vessels (<28 m) 
that fish in shallower waters on the shelf and would most likely 
interact with spiny angel sharks. These vessels saw declines of up to 
58 percent in CPUE of Squatina spp. (of which spiny angel sharks are 
thought to comprise the majority) between the years of 1992 and 1998 
(Massa and Hozbor 2003). In the spring of 2003, the estimated biomass 
of spiny angel sharks for all of coastal Argentina was 23,600 t (Massa 
et al. 2004b). Information about effort was not provided and more 
recent abundance or biomass estimates could not be found.
    In Brazil, there are no biomass estimates for the species and most 
of the fisheries data for angel sharks is grouped into a general 
Squatina spp. category; however, spiny angel sharks are thought to 
comprise the majority of the group (Vooren and da Silva 1991; Cousseau 
and Figueroa 2001; Vooren and Klippel 2005a). Off Rio Grande do Sul 
(between 35[deg] S. and 28[deg] S.), where spiny angel sharks are 
primarily exploited in Brazil, mean annual landings of all angel sharks 
were over 2000 t from 1985 to 1994 but fell to 607 t by 1997. In 1995, 
mortality rates of S. guggenheim exceeded population growth rates 
leading to an annual population decline rate of 16 percent (Vooren and 
Klippel 2005a citing Vieira 1996). Based on CPUE data from fisheries 
operating in this area, the population of S. guggenheim is estimated to 
have declined by 85 percent between 1986 and 2002 (Vooren and Klippel 
2005a). Catches of angel sharks have continued to decline; however, 
landings of both S. guggenheim and S. occulta have been prohibited in 
Brazil since 2004, and this could explain why catches have declined.

Summary of Factors Affecting the Spiny Angel Shark

    We reviewed the best available information regarding historical, 
current, and potential threats to the spiny angel shark. We find that 
the main threat to this species is overutilization for commercial 
purposes. We consider the severity of this threat to be somewhat 
reduced by the species' relatively high abundance in the southern 
portions of its range; however, its demographic characteristics 
(including very low productivity, limited connectivity, and low genetic 
diversity) increase the susceptibility of the species to depletion and, 
with the continued fishing pressure on the species, places it at an 
increased risk of extinction. We summarize information regarding these 
threats and their interactions below according to the factors specified 
in section 4(a)(1) of the ESA. Available information does not indicate 
that habitat destruction or curtailment, disease, predation or other 
natural or manmade factors are

[[Page 76095]]

operative threats on these species; therefore, we do not discuss these 
factors further in this finding. See Casselbury and Carlson (2015e) for 
discussion of these ESA section 4(a)(1) threat categories.

Overutilization for Commercial, Recreational, Scientific, or 
Educational Purposes

    The primary threat to spiny angel sharks is overutilization in 
commercial and artisanal fisheries as the species is heavily fished 
throughout its entire range, including within its nursery grounds. As 
noted previously, the vast majority of fisheries information available 
on angel sharks from Argentina, Uruguay, and Brazil is reported as 
Squatina spp., which includes S. guggenheim, S. argentina, and S. 
occulta. All information in this section that refers to angel sharks 
includes multiple angel shark species, whereas information specific to 
S. guggenheim will specifically reference spiny angel sharks.
    In Argentina, there is no directed fishery for angel sharks, but 
they are captured in multispecies artisanal shark fisheries and are 
considered a valuable bycatch species (Chiaramonte 1998; Bornatowski et 
al. 2011). The spiny angel shark, in particular, is commercially 
exploited in local fisheries that occur in the San Mat[iacute]as Gulf, 
Argentina (Perier et al. 2011), which comprises around 10 percent of 
its range. The species is also commercially exploited by the fisheries 
operating in the AUFCZ, which, based on survey data, overlaps with 
areas of higher concentration of the species (Jaureguizar et al. 2006; 
Colonello et al. 2007; Massa and Hozbor 2008; V[ouml]gler et al. 2008) 
and comprises around 25 percent of the species' range. Angel sharks are 
widely consumed as fresh product called pollo de mar (chicken of the 
sea) and as dried and salted product called bacalao argentino 
(Argentine cod) (Chiaramonte 1998), and in 2007, angel shark export 
revenue in Argentina totaled $2,732,274 U.S. dollars (Argentina FAO 
NPOA-sharks 2009).
    In Argentina, in the 1990s, angel sharks were considered 
commercially important bycatch, particularly in the Necochea school 
shark (Galeorhinus galeus) gillnet fishery. During the 1980s, the 
school shark became an important resource for coastal fisheries, and by 
the 1990s, it was the main shark fishery in the Southwest Atlantic 
(Chiaramonte 1998). As the school shark was traditionally fished using 
gillnets, the fishery also landed significant amounts of demersal angel 
sharks (S. guggenheim and S. argentina), the majority of which were 
gravid females (Chiaramonte 1998). Angel sharks (likely comprised 
primarily of S. guggenheim) became the second most important fish in 
the Necochea artisanal gillnet fishery (Chiaramonte 1998). In fact, 
total declared landings of angel sharks in Argentina between 1992 and 
1996 steadily rose from 1,358.6 mt to 4,281.1 mt with the majority (66 
to 75 percent) of the landings attributed to coastal fishing vessels 
(Chiaramonte 1998). Massa and Hozbor (2003) report even higher landings 
figures for the years of 1992 to 1995, with landings over 3,500 mt and 
totaling more than 14,5000 t for that time period. From 1996 to 1998, 
annual landings of angel sharks reached over 4,000 mt (Massa and Hozbor 
2003). Although landings of angel sharks were relatively high and 
fairly stable throughout the 1990s, there were corresponding decreases 
in CPUE, signifying a decline in the abundance of angel sharks that can 
likely be attributed to overutilization of S. guggenheim. According to 
Massa and Hozbor (2003), the small coastal vessels (<20 m in length), 
which were responsible for the majority of angel shark landings, saw 
CPUE decline from 12 kg/hour in 1992 to around 5 kg/hour by 1998, a 
decrease of around 58 percent. The larger fishing vessels (of 20 m-28 m 
in length and >28 m in length), which focus effort on the inner and 
outer continental shelf (habitat for larger juveniles and adults of the 
species), experienced declines in CPUE of angel sharks of around 44 and 
50 percent, respectively (Massa and Hozbor 2003).
    Current fishing pressure remains high on the spiny angel shark in 
Argentinian waters. In fact, recent landings of angel sharks, and just 
from the AUCFZ portion of the species' Argentinian range, suggest total 
Argentinian landings have likely been of similar magnitude as those 
totals reported in the 1990s (CTMFM 2015). In 2010, total landings in 
the AUCFZ amounted to 3,763 t and were over 3,000 t in 2011. In 2012, 
landings were 2,736 t and by 2013 and 2014 dropped to below 2,300 t 
(CTMFM 2015). Although landings have remained high in recent years, 
they also appear to be on a declining trend. Given that catch levels in 
the 1990s, which resulted in declines of up to 58 percent in the 
species' abundance, remained at similar levels in 2010 and 2011, 
suggests that the decrease in landings may likely be a result of a 
declining spiny angel shark population as opposed to a decrease in 
fishing effort. In fact, since 2006, the total number of vessels in 
Argentina's fishing fleet has remained fairly stable (OECD 2014), and, 
as of June 2014, there were 635 vessels authorized to operate in the 
AUCFZ, with more than half of these vessels identified as trawlers 
(CTMFM 2015). Additionally, of the 635 vessels, around 20 percent 
identified as coastal vessels, suggesting that fishing pressure and 
associated fishery-related mortality will continue to be a threat to 
all life stages of the species into the foreseeable future.
    In Uruguay, spiny angel sharks are captured by industrial trawling 
fleets in coastal and offshore waters (V[ouml]gler et al. 2008). They 
are bycatch species in bottom longline, estuarine gillnet, and some 
trawl fisheries, but they are also targeted in oceanic gillnet and 
bottom trawl fisheries (Domingo et al. 2008). The Uruguayan artisanal 
and industrial trawling fleets primarily operate at depths between 10 m 
and 200 m, which covers the entire depth range of the spiny angel 
shark. Annual catches of angel sharks in Uruguay were less than 100 t 
from 1977 to 1996 and ranged between 200 t and 400 t between 1997 and 
2005, with the majority likely spiny angel sharks (Domingo et al. 
2008). Currently, Uruguay has a fishing fleet of 62 vessels operating 
within the AUFCZ, with Uruguayan vessels responsible for around 5.6-7.5 
percent of the total angel shark landings from this area from 2010 to 
2013. In 2014, this proportion sharply increased to 18.4 percent as did 
the total number of landings (from 26 t in 2012 to 142 t and 158 t in 
2013 and 2014, respectively) indicating a potential increasing trend in 
the exploitation of the spiny angel shark by Uruguayan fishing vessels.
    In southern Brazil, spiny angel sharks have been heavily fished by 
industrial trawlers and gillnet fleets for the past few decades 
(Haimovici 1998; V[ouml]gler et al. 2008). In fact, mean annual 
landings of all angel sharks (of which the majority were likely S. 
guggenheim) were over 2000 t from 1985 to 1994, with a peak of 2,296 t 
in 1993. Given the depth and distribution of S. guggenheim on the 
Plataforma Sul, (which likely extends from <10 m to up to 150 m depths 
based on species accounts in Argentina; Cousseau 1973; Vooren and da 
Silva 1991; Chiaramonte and Vooren 2007), it is highly susceptible to 
being caught by the various types of industrial fleets operating on the 
continental shelf, including the pair trawl fleet, which primarily 
operates off the coast and on the inner continental shelf (up to depths 
of 100 m), and the simple trawl fleet, which primarily focuses the 
outer continental shelf (in depths of 50 m to <200 m) (Vooren et al. 
2005 a; Klippel et al. 2005). Although S. guggenheim did not appear to 
be a species of interest

[[Page 76096]]

in the mid-1970s, this started to change by the early 1980s. For 
example, in the simple trawl fleet, which operated out of Rio Grande in 
depths of 50 m-100 m and engaged in multi-species fisheries directed 
towards bony fishes (Klippel et al. 2005; Vooren and Klippel 2005a), 
the proportion of angel sharks (S. guggenheim and S. occulata) in the 
landings steadily rose from 1975 to 1986. From 1975-1979, the 
proportion of angel sharks in the landings data was estimated to be 3.5 
percent (range: 2.6-4.1 percent) and for the period covering 1980-1986, 
this had increased to 6.2 percent (range: 5.3-7.2 percent) (Vooren and 
Klippel 2005a). Although the simple trawl fleet did not specifically 
target Squatina spp., the increase of angel sharks in landings suggests 
a greater interest in the species and indicates that it was 
incidentally caught and retained during regular fishing operations 
(Vooren and Klippel 2005a). In 1987, the proportion of angel sharks in 
the landings reached a peak of 9.5 percent, which Vooren and Klippel 
(2005a) suggest may be evidence of a directed fishery for the species 
in the simple trawl fleet. However, after 1987, the angel shark 
proportion in the landings significantly decreased, dropping to 5.4 
percent in 1990 and 0.5 percent by 2001 (Vooren and Klippel 2005a). The 
CPUE of angel sharks (S. guggenheim and S. occulata) by the simple 
trawl fleets also decreased over this time period, from an average of 
2.75 t/trip (range: 2.59-3.02 t/trip) from 1980-1988 to 0.41 t/trip 
(range: 0.26-0.62 t/trip) over the years 1997-2002. This 85 percent 
decrease in CPUE of the species suggests that the declining trend in 
the landings data was likely indicative of overexploitation that led to 
a decline in the species' abundance in the fishing area where these 
fleets operate (Vooren and Klippel 2005a). Additionally, given that 
CPUE of angel sharks (S. guggenheim and S. occulata) in the Rio Grande 
pair trawl fleet also declined over this time period, the decrease in 
abundance of angel sharks was likely widespread over the continental 
shelf. In the pair trawl fleet, CPUE decreased from 0.94 t/trip (range: 
0.34-1.39 t/trip) to 0.12 t/trip (range: 0.08-0.17 t/trip) between the 
periods of 1980-1988 and 1997-2002, a decline of 87 percent (Vooren and 
Klippel 2005a). In 1995, it was estimated that the fishing mortality 
rate of S. guggenheim had exceeded its population growth rate, 
resulting in an annual rate of population decline of 16 percent (Vooren 
and Klippel 2005a citing Vieira 1996). Based on the above data, as well 
as data from fishery research surveys, Vooren and Klippel (2005a) 
estimate that the S. guggenheim population on the Plataforma Sul 
decreased by around 85 percent between 1986 and 2002, with the decline 
occurring simultaneously with the increase in fishing effort and caused 
by overexploitation of the species.
    However, spiny angel sharks are not only at risk of fishing 
mortality from the industrial trawl fleets operating on the Plataforma 
Sul, but also from the commercial oceanic gillnet fisheries which began 
expanding in the 1990s. As the trawl fleets saw catches start to 
decline, due to the overexploitation of the marine resources, many 
trawlers began converting their boats to gillnet vessels in the early 
1990s. These vessels would fish at depths of up to 300 m, with the 
oceanic bottom gillnet fishermen specifically targeting sharks and, 
based on CPUE data, potentially Squatina species (Miranda and Vooren 
2003). The number of gillnet vessels as well as fishing effort 
increased throughout the 1990s, with annual landings of angel sharks by 
the oceanic gillnet fleet of more than 800 t between the years 1992 to 
1998 (Klippel et al. 2005). Mazzoleni and Schwingel (1999; cited by 
Klippel et al. 2005) report that landings of the three angel shark 
species (S. guggenheim, S. occulta and S. argentina) were common in the 
Santa Catarina bottom gillnet fleet operating on the Plataforma Sul 
between 1994 and 1999. However, from 1999 to 2002, annual landings of 
angel sharks had dropped in half (Klippel et al. 2005). The CPUE of the 
fleet also decreased, from a maximum of 4.3 t/trip in 1992 to values 
that varied between 0.5 t/trip and 1 t/trip in the following years 
(from 1994-2002; Klippel et al. 2005).
    Likely contributing to the decreases in CPUE seen in both the 
industrial trawl and gillnet fleets is the fact that the majority of 
landings from these fisheries consist of juvenile angel sharks which, 
after spending their first year in depths <20 m, migrate out over the 
continental shelf (see Historical and Current Distribution and 
Population Abundance section). In an examination of landings at the 
Port of Rio Grande between June 2002 and July 2003, Klippel et al. 
(2005) found that around 70-85 percent of the spiny angel sharks were 
juveniles (TL <72 cm). The proportion of juveniles was highest in the 
landings from the double-rig trawl fleet, which is to be expected as 
the fleet primarily operates in depths <50 m (Klippel et al. 2005). 
However, the proportion of juveniles was still high, around 70 percent, 
in the landings of the bottom gillnet, pair, and single trawl fleets, 
which operate from the coast to depths >200 m (Klippel et al. 2005). 
The removal of primarily juveniles from a population can have 
significant negative impacts on recruitment, especially for a species 
with a 3-year reproductive cycle. And, in fact, in a 2005 bottom trawl 
survey conducted in the coastal waters of the Plataforma Sul between 
Torres and Chu[iacute], only neonate spiny angel sharks were caught, 
despite the fact that both juveniles and adults would be expected 
within the trawled depth range (7 m-20 m) (Vooren et al. 2005b). The 
CPUE of S. guggenheim was also low compared to historical estimates, 
with an estimate of only 0.18 kg/h (Vooren et al. 2005b).
    Despite the decreases observed in spiny angel shark abundance on 
the Plataforma Sul, fishing effort remains high. Additionally, all life 
stages of spiny angel sharks are susceptible to the industrial shelf 
fisheries as the fleets operate year round covering the entire depth 
distribution of the species. In fact, in 2002, it was estimated that 
the fishing effort of the industrial trawl fleet from Rio Grande do Sul 
and Santa Catarina (the two largest fishing fleets operating on the 
Plataforma Sul) trawled around 141,000 km\2\, corresponding to 
approximately 50 percent of the land area of the state of Rio Grande do 
Sul (Klippel et al. 2005). Hypothetically, if the area swept by each 
trawl vessel was different, the 100,907 km\2\ of the Plataforma Sul 
would be completely swept every 9 months (Klippel et al. 2005). When 
considering the number of gillnet vessels, nets, and the total length 
of these nets operating on the Plataforma Sul, it was estimated that 
the length of these gillnets (combined) would equate to around 8,250 
km, which corresponds to approximately the entire length of the 
Brazilian coast (Klippel et al. 2005). In 2002, a total of 892 t of 
angel sharks were landed, with 62 percent landed in Santa Catarina and 
38 percent in the Rio Grande do Sul. The oceanic gillnet fleet was 
responsible for most of the landings (42 percent), followed by double-
rig trawl fleet (25 percent), and the coastal gillnet, pair, and single 
trawl fleets, which each contributed about 10 percent of the landings 
(Klippel et al. 2005). These fleets, which historically contributed to 
the decline in S. guggenheim on the Plataforma Sul, remain active 
today.
    Furthermore, as previously discussed in the other species 
assessments, these fleets operate at high efforts on the Plataforma Sul 
and especially within important coastal nursery and inner shelf 
habitats for the species. Although landings of the species are 
currently prohibited, the fleets' extensive operations will continue to 
contribute to the fishing mortality of all life stages of

[[Page 76097]]

the species as the spiny angel shark likely has high discard mortality 
rates based on rates estimated for similar angel shark species. For 
example, the at-vessel mortality rate reported for the African 
angelshark (S. africana) is 60 percent in prawn trawlers (Fennessy 
1994) and 67 percent in protective shark gillnets (Shelmerdine and 
Cliff 2006). For the Australian angel shark (S. australis), mortality 
rate estimates of 25 percent and 34 percent have been reported for 
sharks caught in gillnets (Reid and Krogh 1992; Braccini et al. 2012). 
These two angel shark species have similar life history traits and 
ecology, including: Reproductive characteristics (ovoviviparous and 
produce small litters; Compagno 1984; Rowling et al. 2010), maturity 
and maximum sizes (Compagno 1984), depth distribution (continental 
shelf and upper slope), behavior, and diet (mainly teleosts; 
Shelmerddine and Cliff 2006; Rowling et al. 2010). Given the general 
similarities, it seems reasonable to infer similar discard survival 
rates for the spiny angel shark from these other two Squatina species. 
As such, given the sensitive life history traits of the spiny angel 
shark as well as the evidence of significant population declines, an 
assumed 60 percent at-vessel mortality rate in trawl fisheries and 25-
67 percent mortality in gillnets is likely to significantly contribute 
to the overutilization of the species and increase its extinction risk.
    These industrial trawl and gillnet fleets currently participate in 
nationally important fisheries and, as such, the threat they pose to S. 
guggenheim is unlikely to decrease in the foreseeable future. In fact, 
in the oceanic drift gillnet fishery, the fishery responsible for the 
highest landings of angel sharks, the main fish species targeted 
(Umbrina canosai, Cynoscion guatucupa, and Micropogonias furnieri) 
represented around 12.8 percent of the total national marine fish 
landings in 2011 for all of Brazil. Micropogonias furnieri is the 
second most landed fish nationally, and U. canosai is the seventh most 
landed. Based on the above information, the significant level of 
fishing effort and associated fishing mortality, especially of juvenile 
angel sharks, likely caused and will continue to cause substantial 
declines in the spiny angel shark population.

Inadequacy of Existing Regulatory Mechanisms

    In the AUCFZ, the area comprising around one quarter of the 
species' range, and where survey data suggest the species is likely at 
highest concentration (Jaureguizar et al. 2006; Colonello et al. 2007; 
Massa and Hozbor 2008; Vogler et al. 2008), spiny angel sharks are 
commercially exploited. Similar to the narrownose smoothhound, the 
CTMFM manages this exploitation through the implementation of catch 
limits and fishery closures. As stated previously, the CTMFM implements 
an annual prohibition against demersal trawling in a large section of 
the AUCFZ, extending across the continental shelf, in order to protect 
vulnerable chondrichthyans from fishery-related mortality. The CTMFM 
also establishes additional area closures to trawling gear throughout 
the year in the AUCFZ to protect other species, with these closures 
also indirectly protecting spiny angel sharks from further fishery-
related mortality from trawl gear. In terms of the direct management of 
spiny angel sharks, since 2012, the CTMFM has set a total permissible 
catch limit for all Squatina spp. at 2,600 t (Res. N[deg] 8/14, Res. 
N[deg] 10/13, Res. N[deg] 10/12). In November 2012, this limit was met 
and landings of Squatina spp. were banned for the month of December 
(Res. N[deg] 13/12). In 2013, an additional reserve of 400 t was 
proposed to be allowed if the 2,600 t limit was reached; however, total 
landings had decreased from the previous year to 2,103 t (CTMFM 2015). 
In 2014 a 10 percent increase in total allowable catch was allowed to 
be added to the limit if the CTMFM saw fit (Res. N[deg] 10/13, Res. 
N[deg] 8/14); but this was unnecessary as landings amounted to only 
2,281 t (CTMFM 2015). In 2015, the CTMFM kept the same limit that was 
implemented in 2014 (2,600 t with an allowance of 10 percent increase; 
Res. N[deg] 07/15). Although McCormack et al. (2007) report that 
elasmobranch quotas and size regulations are largely ignored in 
Argentina and poorly enforced, Squatina landings have been below the 
maximum catch limit in recent years, providing evidence that 
regulations are potentially being followed. However, without effort 
information, it is unclear whether these regulations and the 
corresponding decreases in landings can be attributed to adequate 
control of the exploitation of the species or rather reflects the lower 
abundance of the species from declining populations, or more likely a 
combination of the two scenarios.
    In Uruguay, regulations that likely contribute to decreasing the 
fishery-related mortality of the species include a summer trawling ban 
in 25 m to 50 m depths between La Paloma and Chuy and specific fishery 
area closures in the spring, summer, and autumn on the Uruguayan 
continental shelf, designated to protect juvenile hake (Merluccius 
hubbsi) (Pereyra et al. 2008). Although the depth distribution of the 
spiny angel shark in Uruguayan waters is unresolved, in southern 
Brazilian waters, the species was previously common year-round at 
depths between 10 m and 100 m. Specifically, adults were frequently 
found in waters between 40 m and 100 m during the autumn and winter and 
between 10 m and 40 m in the spring and summer; and both adults and 
juveniles were abundant in depths of 40 m-60 m year-round (Vooren 1997; 
Miranda and Vooren 2003; Vooren and Klippel 2005a). In northern 
Argentina, spiny angel sharks displayed highest abundances on the outer 
coastal shelf between 29 m and 50 m depths (Jaureguizar et al. 2006). 
Using the above depth distribution in areas just north and south of 
Uruguay as a proxy for the species' depth distribution in Uruguayan 
waters, it is likely that the proposed fishery closures and trawling 
bans will provide some level of protection from fishery-related 
mortality, especially during the species' spring/summer migration to 
shallower waters for pupping and potentially mating purposes.
    The spiny angel shark is also listed as a species of high priority 
in Uruguay's FAO NPOA-sharks (Domingo et al. 2008). The plan, as stated 
previously, has set goals to collect the necessary information on its 
priority species in order to conduct abundance assessments, review 
current fishing licenses, and promote public awareness to release 
captured individuals. However, no updated results from the goals and 
priorities of this plan could be found.
    In Brazil, the spiny angel shark is listed on Annex 1 of Brazil's 
endangered species list and classified as critically endangered 
(Directive N[deg] 445). As described in previous species accounts, an 
Annex 1 listing prohibits the catch of the species except for 
scientific purposes, which requires a special license from IBAMA. There 
is also a prohibition of trawl fishing within three nautical miles from 
the coast of southern Brazil, although the enforcement of this 
prohibition has been noted as difficult (Chiaramonte and Vooren 2007). 
In addition, the species is still susceptible to being caught as 
bycatch in the legally permitted coastal gillnet fisheries and offshore 
trawl and gillnet fisheries and vulnerable to the associated bycatch 
mortality (Lessa and Vooren 2007). The spiny angelshark is also listed 
as one of the 12 species of concern under Brazil's FAO NPOA-sharks and 
would benefit from the proposed fishing closures and other

[[Page 76098]]

management measures outlined in the plan. This includes the fishing 
moratorium and marketing ban, which is proposed to be in effect until 
there is scientific evidence that supports population recovery of the 
spiny angel shark. It also suggests that a fishing exclusion area be 
established in the coastal zone (specifically over a large region of 
the coast of Rio Grande do Sul at depths of 20 m) to protect important 
nursery grounds for the species. However, as mentioned previously, the 
plan was only just approved as of December 2014 and will not be fully 
implemented for another 5 years. Thus, the implementation and 
effectiveness of the recommendations outlined in the plan remain 
uncertain, with the best available information indicating that current 
regulatory measures in Brazil to protect vulnerable species are poorly 
enforced.

Extinction Risk

    The best available information provides multiple lines of evidence 
indicating that the S. guggenheim currently faces a moderate risk of 
extinction. Below, we present the demographic risk analysis, threats 
assessment, and the overall risk of extinction for the spiny angel 
shark.

Demographic Risk Analysis

Abundance
    Spiny angel sharks are likely the most abundant angel shark species 
from southern Brazil to Argentina; however, current quantitative 
estimates of abundance of the species throughout its range are 
unavailable. In Argentina, the abundance of spiny angel sharks in the 
San Mat[iacute]as Gulf (which comprises around 9.6 percent of the 
species' range) was estimated to be 192.53 t in 1993. In 2003, the 
estimated biomass of spiny angel sharks for all of coastal Argentina 
was 23,600 t. No other population estimates have been calculated for 
the species. Additionally, between 1981 and 2004, catch rates and 
density estimates for areas off the Argentine continental shelf have 
been variable; however, fishing fleets reported declines of up to 58 
percent in CPUE between 1992 and 1998.
    In Brazil, quantitative information, in the form of CPUE and 
landings data for the fishing fleets operating on the Plataforma Sul, 
is available for all angel shark species, of which S. guggenheim likely 
comprises a majority. These data provide insight into trends in 
abundance of the spiny angel shark in roughly 20 percent of its range. 
Based on a comparison of the CPUE estimates of angel sharks caught on 
the Plataforma Sul in both the single and pair trawl fishing fleets 
over the time periods of 1980-1988 and 1997-2002, the population of S. 
guggenheim off southern Brazil has declined by around 85 percent since 
1985 (Miranda and Vooren 2003; Vooren and Klippel 2005a). More recent 
landings data from the Santa Catarina oceanic gillnet fishery, covering 
the years 2001-2010, show a peak in angel shark landings in 2004 of 340 
mt before significantly dropping, with only 2.6 mt landed in 2010. 
However, in 2004, landings of S. guggenheim along with S. occulta were 
prohibited and, as such, the decline in landings data after 2004 may be 
a reflection of this prohibition.
    Based on the commercial fishery information, it is likely that 
spiny angel sharks have experienced varying levels of population 
decline throughout its range. In the northern half of the species' 
range (off Brazil), the best available information indicates the 
species has undergone rather substantial population declines, with 
evidence of negative population growth rates that led to significant 
decreases in the overall abundance of the species to the point where 
catch rates and observations of spiny angel sharks are extremely low. 
Off Uruguay and Argentina, where reported biomass estimates suggest the 
species was and is likely still most concentrated, the higher abundance 
levels may explain why the magnitude of population decline is estimated 
to be smaller in this portion of the species' range. Therefore, while 
the species may not be of such low abundance such that it is currently 
at risk of extinction, given the high exploitation of the species 
throughout its range and subsequent population decline in the northern 
half, coupled with the species' low productivity, abundance levels will 
likely continue to decline through the foreseeable future to the point 
where it may be a significant contributing factor to the species' 
overall extinction risk.
Growth Rate/Productivity
    There is minimal information on the growth rate and productivity of 
the species. Based on the estimated von Bertalanffy growth parameters, 
the spiny angel shark exhibits rather fast growth rates for a shark 
species (with a growth coefficient (k) of 0.275/year; Vooren and 
Klippel 2005a). Fast growth rates help protect species from extinction 
by allowing species to attain larger sizes at earlier ages, protecting 
it from predation, and also allowing species to attain sexual maturity 
sooner, thereby contributing to population growth. The fast growth 
rates of the spiny angel shark likely led to the species being the most 
common angel shark found in the southwest Atlantic. However, despite 
its fast growth rates, the spiny angel shark has a significantly 
lengthy reproductive cycle of 3 years, with a litter size ranging 
between 2 and 8 pups and an average of around 4-5 pups/litter. This 
translates to an annual fecundity between 0.67 and 2.67 pups per year. 
Spiny angel sharks are also thought to have cloacal gestation during 
the latter half of pregnancy, which is thought to be the reason why 
Squatina species are observed easily aborting embryos during capture or 
handling. Given the already low annual fecundity of the species, any 
further loss of embryos would significantly decrease their already low 
reproductive output. Overall, these reproductive characteristics 
suggest the species has relatively low productivity, similar to other 
elasmobranch species, which may hinder the species' ability to quickly 
rebound from threats that decrease its abundance (such as 
overutilization) and render the spiny angel shark more vulnerable to 
extinction in the face of other demographic risks and threats.
Spatial Structure/Connectivity
    The spiny angel shark has a widespread range in the southwest 
Atlantic but is thought to be comprised of smaller, more localized 
populations (Chiaramonte and Vooren 2007); however, information to 
support this is currently unavailable. Information on the connectivity 
among S. guggenheim populations throughout its range is limited. The 
populations occurring on the Plataforma Sul, off southern Brazil, are 
assumed to carry out their entire lifecycle within the same area. This 
behavior indicates that these populations maintain population growth by 
recruiting within each area without producing a necessary excess of 
recruits with the potential to migrate to other areas (Vooren and 
Klippel 2005a). As a result, S. guggenheim populations on the 
Plataforma Sul likely have limited movement and dispersal migration 
between neighboring populations, with migrants having no impact on the 
short term abundance of a population. Based on genetic studies, there 
is also evidence of limited connectivity between populations found in 
other parts of the species' range. For example, genetic analyses of 
individuals found around the Rio de la Plata estuary indicate a high 
level of population genetic structure between the spiny angel sharks 
that occur on the outer shelf and those that are found in the outer 
estuarine and coastal waters (with very few immigrants between these

[[Page 76099]]

populations) (Garcia et al. 2015). In other words, the evidence of 
limited inter-population exchange observed in the species reduces the 
recovery potential for the depleted and small local populations found 
throughout the range, and may increase the risk of local extirpations, 
possibly leading to complete extinction.
Diversity
    A recent genetic analysis using maternally-inherited mitochondrial 
DNA markers from spiny angel sharks in and around the Rio de la Plata 
Estuary (approximately mid point of the species' range) found no 
evidence of population genetic structuring (Garcia et al. 2015). 
However, analyses using biparentally-inherited nuclear recombinant DNA 
genes indicated that there was a remarkably high level of population 
genetic structure between spiny angel sharks found on outer shelf and 
those in the coastal and outer estuarine areas (Garcia et al. 2015). 
The combination of low haplotype and high nucleotide diversity can be 
indicative of a transient bottleneck in the ancestral population, or an 
admixture of samples from small, geographically subdivided populations, 
with the genetic patterns of exchange potentially explained by sex-
biased behavior or long term shifts in spatial and temporal 
environmental variables leading to current displacements (Garcia et al. 
2015). However, overall, the low levels of genetic diversity in spiny 
angel shark populations suggest a vulnerability to overexploitation in 
the southwestern Atlantic Ocean (Garcia et al. 2015) and will likely 
render the spiny angel shark more susceptible to extinction in the face 
of other demographic risks and threats.

Threats Assessment

    The primary threat to S. guggenheim is overutilization in artisanal 
and commercial fisheries. The vast majority of fisheries information on 
angel sharks is generally reported as ``Squatina spp'' throughout 
Brazil, Uruguay, and Argentina; however, spiny angel sharks are thought 
to be the most abundant angel shark species from southern Brazil to 
Argentina and, therefore, likely comprise the majority of the Squatina 
species that are landed.
    In Argentina, although the species is not directly targeted, they 
are caught incidentally in multispecies artisanal shark fisheries and 
are considered a valuable bycatch species (Chiaramonte 1998; 
Bornatowski et al. 2011). Fishery-independent research surveys have 
recorded relatively high densities of the species on the Argentinian 
shelf; however, based on CPUE data, the population saw declines of up 
to 58 percent in the late 1990s. Although exploitation of the species 
in the AUCFZ, where the species appears to be at highest concentration, 
has been managed since 2012 with area closures and catch limits, the 
lack of recent abundance estimates or trends hinders an evaluation of 
the adequacy of current regulatory measures in preventing the 
overutilization of the species from this portion of its range. It is 
important to note that landings prior to 2012 from this area were on 
the same order of magnitude as those reported for all of Argentina and 
which subsequently led to the declines observed in the late 1990s. 
Landings have since decreased since the implementation of the catch 
limits, and appear to be on a declining trend; however, the number of 
fishing vessels authorized to operate in the AUCFZ has remained fairly 
stable, potentially indicating that fishing effort has not decreased 
substantially in recent years. In other words, the recent declining 
trend in landings, even below total allowable catch limits, may 
indicate decreasing abundance of the species in this part of its range.
    In Uruguay, spiny angel sharks are both targeted and caught as 
bycatch by industrial trawling fleets in coastal and offshore waters 
(V[ouml]gler et al. 2008; Domingo et al. 2008). All life stages of the 
species are exploited as the fleets operate over the entire depth range 
of the species (between 10 m and 200 m). Abundance and trends of the 
species within this region are unknown; however, declines in 
populations just north and south of this region have been observed, 
with the species listed as high priority in Uruguay's FAO NPOA-sharks. 
Additionally, landings of angel sharks by Uruguayan vessels in the 
AUCFZ have increased in both number and proportion of total angel shark 
landings in the AUCFZ, indicating a potential increase in fishing 
effort of this vulnerable species.
    In Brazil, spiny angel sharks have been heavily exploited by 
industrial trawlers and gillnet fleets since the 1980s (Haimovici 1998; 
V[ouml]gler et al. 2008). In southern Brazil, angel shark landings are 
recorded in industrial single trawl, pair trawl, oceanic bottom 
gillnet, and coastal artisanal fisheries. These industrial and coastal 
artisanal fleets operate year round in depths that span <20 m to 300 m, 
including during the sharks' reproductive seasonal migrations, and 
hence capture all life stages of spiny angel sharks (Vooren and Klippel 
2005a). The impact of this fishing pressure and effort led to observed 
declines in S. guggenheim (around 85 percent), with fishing mortality 
rates exceeding population growth rates and resulting in an annual rate 
of population decline of 16 percent for spiny angel sharks in the mid 
1990s (Vorren and Klippel 2005a). Although many trawlers began 
converting their boats to gillnet vessels in the early 1990s (due to 
decreases in catch), the threat of overutilization remains as the 
oceanic bottom gillnet fishermen also fish at depths of up to 300 m and 
now land the majority of angel sharks, of which 70-85 percent are 
juveniles (Klippel et al. 2005). Although spiny angel sharks have been 
a prohibited species since 2004, the fishing effort (both by trawl and 
gillnet fleets) on the Plataforma Sul remains high and poorly 
regulated, and, therefore, the susceptibility of the species' to 
fishery-related mortality also remains high. The industrial gillnet and 
trawl fleets, which contributed to the historical decline in the 
population off southern Brazil, are active today and participate in 
nationally important fisheries. Given the percentage of juveniles 
caught by these fisheries coupled with the assumed discard mortality 
rates, the continued operations of these fleets will likely have 
significant negative impacts on S. guggenheim recruitment to the 
population, especially for a species with a 3-year reproductive cycle. 
The present level of fishing effort by the artisanal and industrial 
fisheries on Brazil's continental shelf will continue to lead to 
declines in the spiny angel shark population and, hence, contribute to 
the extinction risk of the species.

Risk of Extinction

    There is significant uncertainty regarding the current abundance of 
the species throughout its entire range. While the Brazilian 
populations have experienced substantial declines and remain at risk 
from overutilization by fisheries, the same cannot be concluded with 
certainty for the populations farther south in the species' range. 
Based on the available data, the populations off Uruguay and Argentina 
have likely experienced moderate declines, with recent landings and 
vessel data potentially indicating a decreasing trend in abundance and 
stable or increasing trend in fishing effort. The significant 
demographic risks to the species (e.g., extremely low fecundity, 
declining population growth rate, and limited connectivity), the 
decline and subsequent rarity of the species in an area that comprises 
around half of its range, and the evidence of continued and heavy 
fishing pressure on the species throughout its entire range, place the 
species on a trajectory indicating that it will more likely than

[[Page 76100]]

not be at a high level of extinction risk in the foreseeable future. 
Therefore, based on the best available information and the above 
analysis, we conclude that S. guggenheim is presently at a moderate 
risk of extinction throughout its range.

Protective Efforts

    With the exception of the recommendations within the FAO NPOA-
sharks discussed above, we were unable to find any other information on 
protective efforts for the conservation of spiny angel sharks in 
Argentina, Uruguay, or Brazil that would potentially alter the 
extinction risk for the species. We seek additional information on 
other conservation efforts in our public comment process (see below).

Proposed Determination

    Based on the best available scientific and commercial information 
as presented in the status review report and this finding, we find that 
the spiny angel shark is not presently in danger of extinction 
throughout its range but likely to become so in the foreseeable future. 
We assessed the ESA section 4(a)(1) factors and conclude that the 
species faces ongoing threats from overutilization and inadequacy of 
existing regulatory mechanisms throughout its range. Due to the 
species' relatively fast growth rate (for elasmobranchs) and high 
biomass in the southern portion of its range, the species has not yet 
declined to abundance levels that would likely trigger the onset of 
depensatory processes. However, the species' demographic risks 
(including very low fecundity, low genetic diversity, and connectivity) 
coupled with the significant reduction in the population from the 
northern portion of its range, greatly increases the species' 
vulnerability to extinction from environmental variation or 
anthropogenic perturbations. Furthermore, given the evidence of 
decreasing landings despite stable (or even increasing) fishing effort, 
we find that the level of exploitation in the area where spiny angel 
sharks are currently most concentrated is likely contributing to 
unsustainable fishing mortality rates. We therefore conclude that the 
species is on a trajectory indicating that it will more likely than not 
be at risk of extinction in the foreseeable future. We also found no 
evidence of protective efforts for the conservation of spiny angel 
sharks that would reduce the level of extinction risk faced by the 
species. We therefore propose to list the spiny angel shark as a 
threatened species.

Argentine Angel Shark (Squatina argentina)

Species Description

    In addition to the spiny angel shark, the Argentine angel shark was 
petitioned for listing under the ESA. The Argentine angel shark occurs 
in the Southwest Atlantic and can be distinguished from its sympatric 
species by its coloration, dental formula, neurocranial features, 
dorsal surface denticle pattern, and pectoral fin shape. Unlike S. 
guggenheim, the Argentine angel shark lacks a dorsal midline of 
morphologically distinct denticles (Vaz and Carvalho 2013). Dermal 
denticles densely cover the entire dorsal surface, except for the 
posterior margins of unpaired fins and the anterior apex of the 
pectoral fins. The pectoral fins are large, twice as long as they are 
wide, with the anterior margins strongly convex, creating a visible 
``shoulder'' area at the base of the head (Vaz and Carvalho 2013). The 
dorsal coloration is dark to purplish brown with small, round, white 
spots symmetrically distributed across the entire dorsal surface 
(Vooren and da Silva 1991; Milessi et al. 2001; Vaz and Carvalho 2013). 
Small individuals are creamy white over the entire ventral surface, 
while larger animals develop dark beige on the central region of the 
head, margins of the pectoral fins, origin of the pelvic fins, and the 
posterior region of the trunk (Vaz and Carvalho 2013). Unlike S. 
guggenheim and S. occulta, female Argentine angel sharks have two 
functional ovaries, which can also serve as an identifying feature 
(Vooren and da Silva 1991).

Range and Habitat Use

    While there is some conflicting information regarding the range of 
Argentine angel shark, it is clear that they have a restricted range in 
the Southwest Atlantic, and are present in southern Brazil (from Rio de 
Janeiro southward), Uruguay, and at least the northern part of 
Argentina (i.e., Buenos Aires). Argentine angel sharks live on muddy or 
sandy bottom substrates on the continental shelf and slope at depths 
between 100 m and 400 m, with a principal depth range of 120 m-320 m 
(Cousseau 1973; Vooren and da Silva 1991; Vooren and Klippel 2005a). 
Angel sharks are active mostly at night, and show limited movement and 
dispersal migration between neighboring populations, with migrants 
having no impact on the short term abundance of a population (Vooren 
and Klippel 2005a).

Diet and Feeding

    Like the spiny angel shark, the Argentine angel shark is thought to 
be a sit-and-wait predator, lying motionless on the bottom until prey 
passes closely overhead. The prey is then grasped by an upward bite 
(Vooren and da Silva 1991). There is limited information regarding the 
Argentine angel shark diet. In a study that analyzed stomach contents 
of 53 individuals, results showed that fish made up 68.33 percent of 
the diet, and crustaceans and molluscs made up 15 percent and 1.6 
percent of the diet, respectively (Cousseau 1973). The rest of the diet 
contained unidentifiable remains. The most common fish species was 
Cynoscion striatus, while the shrimp Artemesia longinaris and 
Hymenopenaeus mulleri were the most common crustaceans, and Loligo 
brasiliensis was the most common mollusc (Cousseau 1973). Argentine 
angel sharks are also thought to occasionally consume the short-finned 
squid (Illex argentinus) (dos Santos and Haimovici 2000).

Growth and Reproduction

    Little is known about the growth and reproduction of the Argentine 
angel shark. Their maximum total length is estimated at 138 cm with a 
size at sexual maturity of 120 cm TL; however, age at first maturity 
and size at birth are unknown (Vooren and da Silva 1991; Vooren and 
Klippel 2005a). Gravid females and neonates are rarely found, so little 
is known about the reproductive characteristics of the species. 
Gestation is lecithotrophic (developing embryos depend on yolk for 
nutrition) (Vooren 1997) and litter size ranges from 7-11 pups (most 
commonly 9 or 10 pups) (Vooren and Klippel 2005a). Like S. occulta and 
S. guggenheim, the Argentine angel shark may have cloacal gestation 
during the latter half of pregnancy (Vooren and Klippel 2005a). Based 
on the location and capture of two neonates of 35 cm and 37 cm TL in 
Santa Catarina, Brazil, it is assumed that Argentine angel sharks 
reproduce on the slope of the southern Brazilian continental shelf 
(Vooren and Klippel 2005a). Additionally, the Bahia Engano in coastal 
Patagonia is thought to serve as a nursery area for the Argentine angel 
shark (Van der Molen et al. 1998).

Genetics and Population Structure

    Studies examining the genetics of the species or information on its 
population structure could not be found.

Demography

    Information regarding natural mortality rates or the intrinsic rate 
of

[[Page 76101]]

population increase of the Argentine angel shark is currently unknown.

Historical and Current Distribution and Population Abundance

    As previously described, there is conflicting information regarding 
the range of the Argentine angel shark, and the species' distribution 
is poorly defined. While there are no specific population abundance 
estimates for Argentine angel sharks, they are considered to be the 
least common species of angel shark found in the southwestern Atlantic, 
particularly in Argentina (Vooren and Klippel 2005a). According to one 
paper, Argentine angel sharks occur in highest densities (from 1 to 
11.4 t/nm\2\) along the Uruguayan coast in the AUCFZ, where salinities 
are higher than the Argentine coast (D[iacute]az de Astarloa et al. 
1997). However, this paper refers to all Squatina species as Argentine 
angel sharks and, based on the distribution of S. guggenheim (see 
species assessment; Colonello et al. 2007), the authors have likely 
misidentified spiny angel sharks as Argentine angel sharks.
    In Brazil, Argentine angel sharks of all life stages are most 
abundant between Rio Grande and Chu[iacute] in Rio Grande do Sul, with 
no evidence of abundant populations outside of this area (Vooren and 
Klippel 2005a; Vooren and Chiaramonte 2006). Specifically, the outer 
shelf and upper slope of the southern Brazilian continental shelf, 
south of latitude 32 [deg]S., are important habitat areas for S. 
argentina. However, based on fishery independent research surveys from 
1986-2002, the abundances of both the Argentine angel shark and the 
hidden angel shark (S. occulta) within this area have declined by 
approximately 80 percent (Vooren and Klippel 2005a).

Summary of Factors Affecting the Argentine Angel Shark

    We reviewed the best available information regarding historical, 
current, and potential threats to the Argentine angel shark species. We 
find that the main threat to this species is overutilization for 
commercial purposes. We consider the severity of this threat to be 
exacerbated by the species' natural biological vulnerability to 
overexploitation, which has led to significant declines in abundance of 
the species. We find current regulatory measures inadequate to protect 
the species from further overutilization. Hence, we identify these 
factors as additional threats contributing to the species' risk of 
extinction. We summarize information regarding these threats and their 
interactions below according to the factors specified in section 
4(a)(1) of the ESA. Available information does not indicate that 
habitat destruction or modification, disease, predation or other 
natural or manmade factors are operative threats on these species; 
therefore, we do not discuss these factors further in this finding. See 
Casselbury and Carlson (2015f) for discussion of these ESA section 
4(a)(1) threat categories.

Overutilization for Commercial, Recreational, Scientific or Educational 
Purposes

    The primary threat to S. argentina is overutilization by commercial 
fisheries, particularly the trawl and bottom gillnet fisheries in 
Brazil, where the species is likely most concentrated. As mentioned 
previously, the vast majority of fisheries information on angel sharks 
is documented as ``Squatina spp'' throughout Brazil, Uruguay, and 
Argentina; however, the Argentine angel shark is the rarest Squatina 
species in the region. Additionally, incorrect species identification 
of angel sharks is a problem that persists in the AUCFZ, particularly 
in Argentine landings (Milessi et al. 2001); therefore, determining the 
magnitude of threats currently acting specifically on S. argentina is 
challenging. However, some information, including fisheries effort, 
catch and landings data, provides insight into the current status of 
Argentine angel shark, as described below.
    As discussed in the spiny angel shark assessment, angel sharks, in 
general, have been historically caught in the multispecies artisanal 
shark fisheries and considered valuable bycatch species in Argentina 
(see spiny angel shark: Overutilization section). However, the 
Argentine angel shark is considered relatively rare in Argentina (Menni 
et al. 1984 cited in Vooren and Klippel 2005a), with S. guggenheim 
comprising the majority of the catch (Massa et al. 2004b). From 1981-
1982, Otero et al. (1982) noted the low density of S. argentina off the 
Buenos Aires coast and estimated an annual biomass of only 4,050 t. In 
the 1990s, angel sharks became commercially important bycatch, 
particularly in the Necochea school shark (Galeorhinus galeus) gillnet 
fishery, and were a prevalent bycatch species in the Patagonian coastal 
trawl fisheries. According to 1993-1996 observer data from the 
Patagonian fishery, Argentine angel sharks were bycaught with medium 
frequency, particularly in the San Matias Gulf and Bahia Engano. By 
1993, declared landings of S. argentina were on the same order of 
magnitude as the total biomass of the population estimated from the 
early 1980s, at 3,974.7 mt, and landings remained near this level in 
1994 at 3,621.8 mt (Chiaramonte 1998). However, by 1998, CPUE values 
indicated that the level of fishing mortality on the Squatina shark 
populations was leading to declines in abundance of angel sharks. 
Specifically, Massa and Hozbor (2003) estimated that CPUE of angel 
sharks declined by 58 percent between 1992 and 1998 for vessels 
operating on the Argentine shelf, and since 1998, landings of Squatina 
species have been on a decline (Massa et al. 2004b).
    In Uruguay, Argentine angel sharks are targeted in the Atlantic 
gillnet fishery and bottom trawl fisheries. They are also caught as 
bycatch in bottom longline, estuarine gillnet, and bottom trawl 
fisheries (Domingo et al. 2008). Both artisanal and industrial trawl 
fleets operate at depths between 10 m and 200 m in Uruguay, which 
overlap with the principal depth range of S. argentina. Annual catches 
of all angel sharks in Uruguay have increased over time, with less than 
100 t landed from 1977 to 1996 and increasing to between 200 t and 400 
t from 1997 to 2005. In 2012, catches for Squatina spp. exceeded the 
set catch limit in the AUCFZ (2,600 t), resulting in the closure of the 
fishery for the following month. However, similar to catch composition 
reported in Argentina, it is likely that the majority of these reported 
angel shark landings are spiny angel sharks rather than Argentine angel 
sharks (Domingo et al. 2008).
    In Brazil, Argentine angel sharks are most abundant between Rio 
Grande and Chu[iacute] in Rio Grande do Sul, off southern Brazil 
(Vooren and Klippel 2005a; Vooren and Chiaramonte 2006); however, they 
are the least captured Squatina species in Brazilian fisheries (Perez 
and Wahlrich 2005). In general, angel shark landings are recorded in 
single trawl, pair trawl, oceanic gillnet, and coastal artisanal 
fisheries. Historically, angel sharks were fished on the Brazilian 
shelf by double rig trawlers down to 140 m depths, with S. guggenheim 
comprising the majority of the catch (Haimovici 1998).
    As catch rates of shelf resources decreased, and international 
markets for traditionally discarded or poorly known species expanded, 
deep-water demersal fishing operations off southern Brazil (from 
20[deg] S.-34[deg] S.) increased in the early 1990s (Valentini et al. 
1991; Haimovici 1998) and greatly accelerated after 1999. This was 
largely a result of shrimp and groundfish trawlers expanding their 
fishing grounds towards the previously unexploited resources of

[[Page 76102]]

the outer shelf and slope (Valentim et al. 2007; Perez and Wahrlich 
2005), but also reflected the increasing number of gillnet vessels 
operating on the outer shelf. In fact, in the early 1990s, in response 
to a decline in trawl catch of marine resources, many trawlers began 
converting their boats to gillnet vessels. These vessels would fish at 
depths of up to 300 m, with the oceanic bottom gillnet fisheries 
specifically targeting sharks and, based on CPUE data, potentially 
Squatina species (Miranda and Vooren 2003). The number of gillnet 
vessels as well as fishing effort increased throughout the 1990s, with 
annual landings of angel sharks by the oceanic gillnet fleet of more 
than 800 t between the years 1992 to 1998. Landings of the three angel 
shark species (S. guggenheim, S. occulta and S. argentina) were 
especially common in the Santa Catarina bottom gillnet fleet operating 
on the Plataforma Sul between 1994 and 1999 (Mazzoleni and Schwingel 
1999; cited by Klippel et al. 2005). However, in the following years, 
from 1999 to 2002, annual landings of angel sharks dropped in half and 
the CPUE of the bottom gillnet fleet also decreased, from a maximum of 
4.3 t/trip in 1992 to values that varied between 0.5 t/trip and 1 t/
trip in the years 1994-2002 (Klippel et al. 2005).
    As the regional Brazilian fleets gradually occupied slope grounds 
in the 1990s, they were joined by foreign fleets chartered by national 
companies as part of a deep-water fishing development program promoted 
by Brazilian authorities (Perez et al. 2003). This program was 
implemented in 2000, with chartered vessels operating at depths of 200 
m to 900 m in the Brazilian EEZ, using traps, longlines, gillnets, and 
trawl nets (Perez and Pezzuto 2006 cited in Perez et al. 2009). 
Together, both national and foreign trawlers concentrated their efforts 
in the southern and southeastern sectors of the Brazilian coast, 
exploiting three discrete bathymetric strata: shelf break (100-250 m), 
upper slope (250-500 m), and lower slope (> 500 m) (Perez and Pezzuto 
2006 cited in Perez et al. 2009). Brazilian trawlers concentrated their 
activities on the shelf break (at 100-200 m) while chartered gillnet 
vessels concentrated their efforts in deeper areas of the upper slope 
(at 300-400 m). As a result of this expansion of fishing activities 
into deeper waters, deep-water monkfish (Lophius gastrophysus) was the 
first fishing resource that proved abundant enough to sustain 
profitable deepwater fishing operations off southern Brazil, and thus a 
targeted fishery developed for the species. In 2001, a total of 7,094 t 
of monkfish were landed, mostly by national double-rig trawlers (58 
percent) and foreign chartered gillnetters (36 percent) operating in a 
fishing area that extended along the southern Brazilian slope, from 
21[deg] S. to 34[deg] S. and within the 100-600 m isobaths (Perez et 
al. 2005). Monkfish biomass also happened to be concentrated between 
125 m and 350 m depths, which overlaps with the principal depth 
distribution of the Argentine angel shark (120 m-320 m). As a result, 
Argentine angel sharks were reported as a significant bycatch species 
in the monkfish gillnet fishery. In fact, Perez and Warhlich (2005) 
noted that S. argentina was one of the most retained bycatch species in 
the monkfish gillnet fishery, with bycatch estimated at 1.052 per 100 
nets in 2001 (total 8,698 individuals). This fishing regime that 
contributed to the significant bycatch of Argentine angel shark 
continued operating at high levels through most of the following year 
(2002), with monkfish landings of 5,129 t (Perez et al. 2009). The 
numerous incidental catches produced by monkfish gillnetting suggests 
that the development of this fishery off southern Brazil substantially 
increased the levels of fishery-related mortality in the S. argentina 
population and potentially introduced adverse effects in the 
recruitment process (i.e., recruitment overfishing), especially 
considering that the species' reproductive cycle may exceed 1 year 
(Cousseau and Perrota 1998 cited in Perez and Warhlich 2005). In fact, 
research bottom trawl surveys of the outer shelf and upper slope from 
Cape Santa Marta Grande to Chu[iacute] (the main habitat of Argentine 
angel sharks) found decreases in both the CPUE and frequency of 
occurrence of Argentine angel sharks during the winter and fall seasons 
between the years 1986/87 and 2001/02. Specifically, these surveys 
detected declines of 75 and 96 percent in S. argentina CPUE (kg/hour) 
and frequency of occurrence, respectively, during the winter months, 
and declines of 97 and 63 percent, respectively, during the fall 
surveys. These declines confirm that the abundance of S. argentina in 
southern Brazil decreased by roughly 80 percent from its original level 
as a result of recruitment overfishing, primarily due to the bottom 
gillnet fishery (Vooren and Lam[oacute]naca 2002; Vooren and Klippel 
2005a).
    In 2003, the fishery regime changed, as the foreign chartered 
vessels abandoned Brazilian waters as a result of conflicts with 
national trawlers (Perez et al. 2009). Since then, exploitation has 
been maintained mostly by double-rig trawlers along with a few vessels 
of the national fleet transformed to fish with the new gillnet 
technology (Wahrlich et al. 2004 cited in Perez et al. 2009). Landings 
of monkfish decreased by roughly 50 percent from 2002 to 2003, and have 
remained stable around 2,500 t ever since (Perez et al. 2009). The 
large reduction in monkfish biomass after 2002 (and the stabilization 
at biologically insecure levels thereafter) is largely attributed to 
the fact that landed catches have been systematically higher than 
maximum recommended catches (Perez, 2007a; Anon 2007 cited in Perez et 
al. 2009). In 2004, the monkfish fishery was declared overexploited, 
with subsequent biomass assessments lacking any signs of recovery for 
the monkfish stock (Perez et al. 2009). Given the significant bycatch 
of Argentine angel sharks in the monkfish fishery in 2001, and the 
subsequent 80 percent decline in the angel shark population by 2002, 
the continued intense exploitation by the monkfish fishery within the 
Argentine angel shark habitat likely contributed to further abundance 
declines of S. argentina after 2002. This is especially probable 
considering the fact that the fishery operates on the outer and upper 
slope areas of the continental shelf, where the Argentine angel shark 
reproduces and likely carries out its entire lifecycle. Thus, the 
significant increase in fishing effort on the outer shelf and slope 
areas, particularly by the monkfish fishery, likely impacted all life 
stages of the species, resulting in recruitment overfishing and, 
ultimately, overutilization of the species leading to a significant 
population decline.
    Argentine angel sharks are still likely susceptible to fishing 
pressure in the monkfish fishery, as the fishery is still operational 
today. Recent landings of monkfish for years 2009, 2010, and 2011 were 
2,744 mt, 2,592 mt and 2,616 mt, respectively (IBAMA 2011). While this 
is a large reduction from peak landings in 2001 of 7,094 mt, Argentine 
angel sharks of all life stages are likely still bycaught by this 
fishery, which may limit the species from recovering from its initial 
80 percent population decline, especially considering the species' low 
productivity. In addition, the Argentine angel shark likely has high 
discard mortality rates based on rates estimated for similar angel 
shark species (see spiny angel shark--Threats Assessment). Given 
general similarities between the Argentine angel shark and other 
Squatina species, it seems reasonable to infer similar discard survival 
rates for the Argentine angel shark (i.e., ~60 percent at-vessel

[[Page 76103]]

mortality rate in trawl fisheries and ~25-67 percent mortality in 
gillnets).
    Thus, while the bottom gillnet fishery specifically targeting 
monkfish has been restricted in terms of overall effort, with only the 
national trawl fleet continuing to operate on the upper slope (Perez et 
al. 2009), the threat of overutilization remains. However, the monkfish 
fishery is not the only fishery presently operating within the 
Argentine angel shark habitat. There are a number of oceanic bottom 
gillnet fisheries targeting other species (e.g., Umbrina canosai, 
Cynoscion guatucupa, and Micropogonias furnieri) that currently operate 
on the shelf and slope at depths of up to 300 m. In fact, due to their 
effort and fishing area of operation, these oceanic bottom gillnet 
fisheries now land the majority of angel sharks in Brazil (Klippel et 
al. 2005). As described in the spiny angel shark assessment, fishing 
effort (both by trawl and gillnet fleets) on the Plataforma Sul remains 
high and poorly regulated, and therefore, the susceptibility of the 
species' to fishery-related mortality also remains high. As such, given 
the best available information and the above analysis, we conclude that 
overutilization is a factor that is significantly contributing to the 
extinction risk of the species.

Inadequacy of Existing Regulatory Mechanisms

    In Argentina, catches of angel sharks are regulated through annual 
catch limits and fisheries closures. Since 2013, Squatina landings have 
been below the maximum catch limit in recent years, providing evidence 
that regulations are potentially being followed. However, without 
effort information, it is unclear whether these regulations are 
adequately controlling the exploitation of angel sharks and given that 
Argentine angel sharks are particularly rare in Argentina, the degree 
to which these regulations are decreasing the threat of overutilization 
of the species in this portion of its range is uncertain.
    In Uruguay, the Argentine angel shark is listed as a species of 
high priority in the country's FAO NPOA-sharks (Domingo et al. 2008). 
The plan, as stated previously, has set goals to collect the necessary 
information on its priority species in order to conduct abundance 
assessments, review current fishing licenses, and promote public 
awareness to release captured individuals. However, no updated results 
from the goals and priorities of this plan could be found.
    Like the spiny angel shark, and other species described previously 
in this proposed rule, the Argentine angel shark was listed as 
``critically endangered'' under Annex I of Brazil's endangered species 
list in 2004. As described in previous species assessments, an Annex 1 
listing prohibits the catch of the species except for scientific 
purposes, which requires a special license from IBAMA. There is also a 
prohibition of trawl fishing within three nautical miles from the coast 
of southern Brazil, although enforcement of this prohibition has been 
noted as difficult (Chiaramonte and Vooren 2007), and moreover, the ban 
only covers depths of <10 m, which does little to provide any 
protection to the Argentine angel shark given its principal depth 
distribution of 120-320 m. As described in previous species 
assessments, Brazil has a FAO NPOA-sharks; however, the Argentine angel 
shark is not considered one of the 12 species of concern.
    Finally, there are some regulatory mechanisms in place for the 
monkfish fishery in Brazil, which operates in the primary habitat of 
the Argentine angel shark and has been a significant source of bycatch-
related mortality for the species. In mid-2002, government regulations 
were implemented to prohibit foreign gillnetters from operating south 
of 21[deg]S (to the southern extent of Brazil's EEZ), which roughly 
encompasses the entirety of the Argentine angel shark's Brazilian 
range. This regulation effectively terminated foreign chartered gillnet 
operations off Brazil and left a national fleet of 5 licensed units to 
continue the fishery (Perez et al. 2009). However, despite this 
reduction of the monkfish fishery fleet, uncontrolled exploitation 
continued and the stock was declared overexploited in 2004. It was not 
until 2005 that a management plan for the monkfish fishery was 
eventually developed, which included the implementation of 100 percent 
observer coverage for monitoring the fishery, logbooks, and a 
recommendation to ban fishing shallower than 250 m (Perez et al. 2009). 
However, the principal depth range of S. argentina exceeds the 250 m 
restriction, thus this recommendation only theoretically protects a 
portion of the species' depth range. In 2008, catch limits of 1,500 t 
per year were imposed for the monkfish gillnet fishery, as well as 
bycatch limits of certain species; however, though the catch limits 
should help reduce overall fishing effort, the species is still 
susceptible to bycatch-related mortality in the fishery.
    Overall, regulatory mechanisms for the monkfish fishery, 
particularly the ban of chartered foreign gillnets from 21[deg] S. to 
the southern extent of Brazil's EEZ, which were responsible for 
catching a total of 157,656 monkfish (compared to a total of only 
16,697 monkfish landed by all gears of the national fleet) from 2000-
2007, and recent catch limits of 1,500 tons for the gillnet fishery, 
have likely reduced the level of fishing pressure and subsequent 
mortality of Argentine angel sharks. However, the fact that enforcement 
of management rules for the monkfish fishery has been poor, with no 
evident signs of recovery for this overexploited resource (Perez et al. 
2009), may indicate that the regulations outlined in the management 
plan for the monkfish are inadequate to control for indirect 
overutilization of Argentine angel sharks. Given that the conservation 
status of the Argentine angel shark likely relies heavily upon the 
success of the management plan for the southern Brazil gillnet monkfish 
fishery (Vooren and Chiaramonte 2006) and that the monkfish fishery is 
still operational throughout the species' Brazilian range via the 
national fleet, with reportedly poor enforcement of management rules, 
the fishery is likely still exerting fishing pressure and contributing 
to the overutilization of the already at-risk S. argentina population. 
This continued exploitation is concerning for a species that has 
already undergone such significant declines in a critical portion of 
its range, with no indication of a reversal of this trend. As such, we 
conclude that existing regulatory mechanisms to control for 
overutilization of the Argentine angel shark are inadequate, 
particularly in Brazil, where the species is most heavily concentrated 
and utilized.

Extinction Risk

Demographic Risk Analysis

Abundance
    Estimates of population abundance specifically for Argentine angel 
shark (Squatina argentina) throughout its range are not available. 
However, some qualitative information as well as density and biomass 
estimates are available from parts of the species' range. Compared to 
congeners S. guggenheim and S. occulta, the Argentine angel shark is 
the rarest species of angel shark found in the southwestern Atlantic, 
particularly in Argentina. Biomass of S. argentina in Argentina was 
estimated to be 40,000 mt in 1998, although there is high uncertainty 
with this estimate. In Brazil, this species is reportedly most abundant 
between Rio Grande and Chu[iacute] in Rio Grande do Sul, with no 
evidence of abundant populations outside this region. Based on fishery-
independent

[[Page 76104]]

surveys conducted from 1986-2002, abundance of Argentine angel shark 
declined by approximately 80 percent on the outer shelf and upper slope 
of the Plataforma Sul, which is where the highest concentrations of the 
species is located. Due to uncertainties regarding the range and 
distribution of the species, as well as identification issues between 
S. argentina and other Squatina spp. in the region, the current 
abundance of the species cannot be determined at this time. However, 
given the intense year-round fishing pressure from trawl and gillnet 
fisheries within the very restricted range of this rare species, 
combined with the species' presumed low reproductive output, it is 
likely that S. argentina is experiencing continued population declines 
throughout its range, which is significantly contributing to its 
extinction risk.
Growth Rate/Productivity
    There is limited information regarding the growth and reproduction 
of the Argentine angel shark, and information on natural mortality 
rates or the potential intrinsic rate of population increase for the 
species is unavailable. The species has an estimated maximum total 
length of 138 cm with a size at sexual maturity of 120 cm TL, which 
means the species must grow to approximately 87 percent of its maximum 
size before reaching sexual maturity. Gravid females and neonates are 
rarely found, so little is known about the gestation and birth of this 
species; however, litter sizes range from 7-11 pups (with 9-10 pups 
being common) and their reproductive cycle is reportedly at least 
biennial (Vooren and Chiaramonte 2006). These reproductive 
characteristics suggest the species has relatively low productivity, 
similar to other elasmobranch species, which has likely hindered its 
ability to quickly rebound from threats that decrease its abundance 
(such as overutilization) and renders the species more vulnerable to 
extinction. In addition, similar to its congener S. guggenheim, S. 
argentina is thought to have cloacal gestation during the latter half 
of pregnancy, which increases the likelihood that the species will 
abort pups upon capture and significantly decreases their already low 
reproductive output.
Spatial Structure/Connectivity
    The Argentine angel shark has a very restricted range, from Santa 
Catarina, Brazil to northern Argentina (i.e., Buenos Aires). Currently, 
there is no evidence of abundant populations outside of southern 
Brazil. Argentine angel sharks are sedentary, territorial, and assumed 
to carry out their entire lifecycles within the same area. This 
indicates that populations of the species maintain population growth by 
recruiting within each area without producing a necessary excess of 
recruits with the potential to migrate to other areas (Vooren and 
Klippel 2005a). As a result, S. argentina populations reportedly have 
limited movement and dispersal migration between neighboring 
populations, with migrants having no impact on the short term abundance 
of a population. This limited inter-population exchange reduces the 
recovery potential for the depleted and small local populations and may 
increase the risk of local extirpations, possibly leading to complete 
extinction. Given the lack of evidence of abundant populations outside 
of southern Brazil, and the limited connectivity between the 
populations of southern Brazil and populations elsewhere throughout the 
species' range, conservation of the southern Brazilian populations of 
S. argentina is likely critical for the conservation of the taxon as a 
whole. Thus, based on the available information, low dispersal rates 
among populations of S. argentina poses a significant risk of 
extinction to the species.
Diversity
    The loss of diversity can increase a species' extinction risk 
through decreasing a species' capability of responding to episodic or 
changing environmental conditions. This can occur through a significant 
change or loss of variation in life history characteristics (such as 
reproductive fitness and fecundity), morphology, behavior, or other 
genetic characteristics. Although it is unknown if S. argentina has 
experienced a loss of diversity, the significant decline estimated for 
the population in southern Brazil, as well as the likely small 
populations elsewhere throughout its range, and limited connectivity of 
these populations, suggest the species may be at an increased risk of 
inbreeding depression or random genetic drift and could experience the 
fixing of recessive detrimental genes, reducing the overall fitness of 
the species.

Threats Assessment

    The primary threat to S. argentina is overutilization by commercial 
fisheries, with particular vulnerability to trawl and bottom gillnet 
fisheries. As previously mentioned, the vast majority of fisheries 
information on angel sharks is documented as ``Squatina spp'' 
throughout Brazil, Uruguay, and Argentina; therefore, determining the 
magnitude of threats currently acting specifically on S. argentina is 
challenging. However, there are some landings and CPUE data for S. 
argentina, which suggest the historical and continued level of fishing 
pressure has led to significant observed declines in the species.
    Historically, angel sharks, including S. argentina, were caught in 
multispecies artisanal shark fisheries and considered a valuable 
bycatch species. In Argentina, in the 1990s, angel sharks were 
considered commercially important bycatch, particularly in the Necochea 
school shark (Galeorhinus galeus) gillnet fishery, and between 1992 and 
1998, landings of angel sharks in Argentina were fairly stable. 
However, declines in CPUE over this time period (of up to 58 percent) 
were recorded for vessels operating on the Argentine shelf, indicating 
a level of fishing mortality on the angel shark population that was 
leading to declines in abundance, and since 1998, landings have been on 
a decline (Massa et al. 2004b). In Uruguay, catches of angel sharks 
(Squatina spp) have actually been on an increasing trend since the 
1970s, and exceeded the catch limit imposed in the AUCFZ for 2012 
(2,600 mt). However, in both Argentina and Uruguay, Argentine angel 
sharks are relatively rare, with the majority of angel shark landings 
comprised of S. guggenheim. As such, it is unclear whether 
overutilization is significantly contributing to the species' 
extinction risk in this portion of its range.
    Off southern Brazil, angel sharks have been and continue to be 
heavily exploited by the trawl and gillnet fisheries (see the S. 
guggenheim assessment for more details). This heavy exploitation has 
led to observed declines in the abundance of S. argentina on the 
Plataforma Sul as a result of recruitment overfishing (primarily by the 
bottom gillnet fishery targeting monkfish). Given the natural rarity 
and low productivity of the species, these declines (of up to 80 
percent) have placed the Argentine angel shark at an increased risk of 
extinction from stochastic and depensatory processes. In addition, it 
is likely that the population of Argentine angel shark has continued to 
decline (from the 80 percent estimate in 2002) as a result of the 
continued exploitation of the species by the monkfish gillnet fishery 
that continued unabated until 2004, and the present fishing pressure by 
the reduced monkfish fishery and the other oceanic gillnet fisheries 
operating within the species' habitat. Further, few existing 
regulations appear adequate to

[[Page 76105]]

control the overutilization of S. argentina. In the monkfish fishery, 
which catches significant amounts of Argentine angel shark as byatch, a 
management plan was implemented in 2005. Though the monkfish fishery 
has been significantly reduced in terms of overall effort through catch 
limits and fisheries restrictions, enforcement of management rules has 
been poor with no evident signs of recovery for this overexploited 
resource (Perez et al. 2009). Additionally, in 2004, the Argentine 
angel shark was classified as ``critically endangered'' on Brazil's 
endangered species list, which effectively prohibited the catch of this 
species. However, for the most part, there is reportedly minimal 
control of the fisheries operating on the Plataforma Sul, and this 
regulation does not address the threat of bycatch-related mortality of 
the species. Additionally, although landings of the species are 
currently prohibited, the fleets' extensive operations will continue to 
contribute to the fishing mortality of all life stages of the species 
as the Argentine angel shark likely has high discard mortality rates 
based on rates estimated for similar angel shark species (see spiny 
angel shark--Threats Assessment). Thus, given general similarities 
between the Argentine angel shark and other Squatina species, it seems 
reasonable to infer similar discard survival rates for the Argentine 
angel shark from these other Squatina species. As such, given the 
sensitive life history traits of the Argentine angel shark as well as 
the evidence of significant population declines, an assumed 60 percent 
at-vessel mortality rate in trawl fisheries and 25-67 percent mortality 
in gillnets is likely to significantly contribute to the 
overutilization of the species and increase its extinction risk.
    Overall, it is likely that S. argentina has suffered significant 
population declines throughout its restricted range as a result of 
historical and continued overutilization of the species from direct and 
indirect fishing pressure. Given the reduction of the species' 
critically important southern Brazilian population of at least 80 
percent, combined with inadequate regulatory mechanisms in this part of 
the species' range to control the high level of fishing pressure on the 
species, we conclude that overutilization is significantly contributing 
to the species' risk of extinction.

Risk of Extinction

    Although there is significant uncertainty regarding the current 
abundance of the species, it appears that the Argentine angel shark is 
relatively rare outside of southern Brazil, where small, isolated 
populations have experienced substantial declines and remain at risk 
from overutilization by fisheries targeting deep-water monkfish. Best 
available information indicates the species has experienced at least an 
80 percent reduction of its critically important southern Brazil 
population as a result of intense year-round fishing pressure, and will 
continue to decline without adequate protection from overutilization. 
Given the species' restricted range and present rarity throughout the 
range, combined with its limited movement and dispersal between 
populations and low reproductive output, S. argentina is likely 
strongly influenced by stochastic or depensatory processes. This 
vulnerability is further exacerbated by the present threats of 
overutilization and inadequacy of existing regulatory measures that are 
and will continue to significantly contribute to the decline of the 
existing populations (based on its demographic risks), compromising the 
species' long-term viability. Therefore, based on the best available 
information and the above analysis, we conclude that S. argentina is 
presently at a high risk of extinction throughout its range.

Protective Efforts

    Aside from the management goals outlined in the previously 
described FAO NPOA-sharks in Uruguay, we could not find any additional 
information regarding protective efforts for the Argentine angel shark.

Proposed Determination

    Based on the best available scientific and commercial information 
as presented in the status review report and this finding, we find that 
the Argentine angel shark is presently at risk of extinction throughout 
all of its range. We assessed the ESA section 4(a)(1) factors and 
conclude that the species faces ongoing threats from overutilization 
and inadequacy of existing regulatory mechanisms throughout its range. 
The species' present rarity and restricted range, combined with the its 
natural biological vulnerability to overexploitation and demographic 
risks (e.g., low and declining abundance, low productivity, likely 
small and/or isolated populations at an increased risk of random 
genetic drift, and limited dispersal capabilities) are exacerbating the 
negative effects of the aforementioned threats, placing this species in 
danger of extinction. We also found no evidence of protective efforts 
for the conservation of Argentine angel shark that would reduce the 
level of extinction risk faced by the species or otherwise alter its 
current status. We therefore propose to list the Argentine angel shark 
as an endangered species.

Graytail Skate (Bathyraja griseocauda)

Species Description

    The graytail skate, Bathyraja griseocauda, is a member of the genus 
Bathyraja, the most speciose genus of the family Arhynchobatidae 
(McCormack et al. 2007). Physical features of the graytail skate 
include a disc that is rhomboidal in shape (Bizikov et al. 2004), 
brownish in color with traces of darker spots or rings on its dorsal 
surface, and white or yellow coloring on the ventral side (Norman 1937; 
Bigelow and Schroeder 1965). The posterior margins of the pelvic and 
pectoral fins are dusky, and the tail is grayish brown in color (Norman 
1937), with the underside covered in dark spots (Bizikov et al. 2004). 
The dorsal surface is covered in numerous small spinules, but the tip 
of the snout and axils of the pectoral fins lack spinules (Bigelow and 
Schroeder 1965). There are 18-20 strong median spines on the tail that 
begin above the origin of the pelvic fins and extend to the first 
dorsal fin (Norman 1937; Springer 1971; Bizikov et al. 2004). Males 
have alar thorns, curved spines on the outer part of their pectoral 
fins, arranged in rows with 5-7 thorns per row (Bizikov et al. 2004).

Range and Habitat Use

    The graytail skate occurs in Southwest Atlantic waters off the 
coasts of Argentina, Uruguay, Chile, and the Falkland Islands, and in 
the Southeast Pacific off of Chile (S[aacute]ez and Lamilla 2004). They 
have been caught at latitudes as far north as 39[deg] S. in the Pacific 
Ocean and 34[deg] S. in the Atlantic Ocean, and as far south as 60[deg] 
S. in the Southern Ocean on the Antarctic shelf (Bigelow and Schroeder 
1965; Figueroa et al. 1999; S[aacute]ez and Lamilla 2004). A few 
individuals have been captured on the Antarctic continental shelf, 
around the Antarctic Peninsula. There are also unconfirmed records of 
graytail skate in the Southern Ocean in Prydz Bay, Antarctica (GBIF 
2013). If these records are validated, this would extend the range of 
the skate beyond the southwest Atlantic Ocean and eastern Pacific.

Diet and Feeding

    Various studies on graytail skate diet indicate they are 
opportunistic predators that consume a variety of prey items, but 
primarily favor fish. The most extensive study of the diet and feeding

[[Page 76106]]

habits of the graytail skate caught around the Falkland Islands found 
that skates smaller than 50 cm (DW) preyed mostly on benthic gammarid 
amphipods and isopods, such as Serolis spp., whereas skates larger than 
50 cm DW preyed increasingly on fishes (Brickle et al. 2003). 
Subsequent studies off the Falkland Islands have confirmed this 
ontogenetic diet shift (Laptikhovsky et al. 2005). In adult graytail 
skate, fish can make up more than 40 percent of the diet 
(S[aacute]nchez and Mabraga[ntilde]a 2002). Off the coast of Argentina, 
the graytail skate did not consume crustaceans (S[aacute]nchez and 
Mabraga[ntilde]a 2002), which contrasts with data from the Falkland 
Islands.

Growth and Reproduction

    Graytail skates have a lifespan of approximately 28 years, with a 
maximum observed disc width of 130 cm and a maximum weight of 30.4 kg 
(Arkhipkin et al. 2008; Wakeford et al. 2005). Based on vertebral band 
counts from samples collected from along the coast of Argentina, 
B[uuml]cker (2006) calculated the relative growth rate (k) from the von 
Bertalanffy growth equation to be 0.064 year-1 with a 
theoretical maximum size (L[infin]) of 169.9 cm TL and an 
estimated size-at-birth (L0) of 6.1 cm. Arkhipkin et al. (2008), using 
samples collected only off the Falkland Islands, reported a lower 
growth rate (k) of 0.02 year-1, with a maximum theoretical 
size (L[infin]) of 313.4 cm total length. Growth rates of 
graytail skate begin around 5.6 cm/year for the first 9 years of life 
and decline to 4.3 cm/year between 14 and 20 years old (Arkhipkin et 
al. 2008). In comparison, a study of caudal thorn band counts and 
vertebral centra ring counts found that the most accurate von 
Bertalanffy growth parameters came from the vertebral centra with the 
relative growth rate (k) based on vertebrae centra to be 0.033 
year-1 with a theoretical maximum size (L[infin]) 
of 219.7 cm total length (Gallagher 2000). However, based on observed 
size data, these parameters still slightly underestimate growth 
(Gallagher 2000).
    Little is known about the reproduction of the graytail skate 
(S[aacute]nchez and Mabraga[ntilde]a 2002) and available age and growth 
studies from the same region provide conflicting estimates for length 
and age at maturity. For example, in the Falkland Islands, Gallagher 
(2000) estimated a total length at 50 percent maturity of 120.7 cm for 
both sexes, with males and females maturing after 17.6 and 24.8 years 
respectively. Arkhipkin et al. (2008) estimated a total length at 50 
percent maturity to be 108.2 cm for females and 94.5 cm for males, with 
age at maturity of 14 years for males and 17.8 years for females. Based 
on commercial fleet observer and research cruise data collected around 
the Falkland Islands, males reached 50 percent maturity at a disc width 
of 76-77 cm (Agnew et al. 2000; Wakeford et al. 2005). A Falkland 
Islands study of graytail skate suggests that graytail skate females 
may spawn year-round with a weak spawning peak in the spring and summer 
months observed (Arkhipkin et al. 2008). Around the Falkland Islands, 
the spawning grounds of the graytail skate can be found northwest of 
the islands in deep waters, close to the edge of the continental shelf 
between 200 and 300 m deep (Arkhipkin et al. 2008) and in waters south 
of 51[deg] latitude (Dr. Andreas Winter, Falkland Islands Fisheries 
Stock Assessment Scientist, personal communication 2015). Based on 
catches of the smallest skates, it is thought that hatchlings have disc 
widths between 9 cm and 12 cm (Brickle et al. 2003; Arkhipkin et al. 
2008).

Genetics and Population Structure

    Studies examining the genetics of the species or information on its 
population structure could not be found.

Demography

    Little is known about the population growth and natural mortality 
of the graytail skate. However, based on the life history parameters 
described previously, like other elasmobranchs, the graytail skate is a 
K-selected species with slow growth rates and late age at maturity, 
which is indicative of low productivity (Gallagher 2000; B[uuml]cker 
2006; Arkhipkin et al. 2008).

Historical and Current Distribution and Population Abundance

    Graytail skate occur on the continental shelf and slope in the 
southwestern Atlantic Ocean, south of 34[deg] S. and in the 
southeastern Pacific Ocean, south of 39[deg] S. (Figueroa et al. 1999; 
S[aacute]ez and Lamilla 2004). In the Falkland Islands, graytail skate 
are caught in cool, deep waters on the slopes of the continental shelf 
break, making them more common to the west of the islands (Agnew et al. 
1999; Arkhipkin et al. 2008; Arkhipkin et al. 2012). Outside the 
Falkland Islands, on the Patagonian shelf, they are more commonly found 
on the northwestern outer shelf and northern shelf and slope (Figueroa 
et al. 1999; Arkhipkin et al. 2012). In Argentina, graytail skate are 
found on the continental shelf and slope around Argentina south of 
37[deg] S. and 41[deg] S. respectively (McCormack et al. 2007), where 
they exhibit strict stenothermic and stenohaline behavior. In other 
words, the species appears to tolerate very narrow ranges of 
temperature and salinity (Figueroa et al. 1999), with catch data that 
suggest that the species occurs at water temperatures below 6 [deg]C 
(Menni and Lopez 1984; Colonello and Massa 2004) and salinity above 
33.9 psu (Colonello and Massa 2004).
    Throughout their range, graytail skates are found at depths between 
106 m and 1,010 m, but have been caught as shallow as 77 m in Argentine 
waters (B[uuml]cker 2006). Graytail skate are typically most common at 
depths below 300 m (Bigelow and Schroeder 1965; Menni and Lopez 1984; 
Brickle et al. 2003; Laptikhovsky et al. 2005; Wakeford et al. 2005; 
Arkhipkin et al. 2008; Arkhipkin et al. 2012). However, in Argentina, 
the highest density of graytail skate catches was reported at depths of 
120 m on the Argentina platform between 45[deg] S. and 41[deg] S. 
during the late winter and early spring months (Colonello and Massa, 
2004). As graytail skates mature, they display an ontogenetic shift in 
depth preference (Arkhipkin et al. 2008). For example, in Falkland 
Islands waters, hatchlings occupy nursery grounds of approximately 300 
m-350 m depth, but transition to deeper waters of 400 m-600 m as 
juveniles (Arkhipkin et al. 2008). At 20 cm-30 cm DW, some individuals 
migrate up to shallower depths of 200 m-400 m, while others move into 
water deeper than 600 m (Arkhipkin et al. 2008). Skates 80 cm-90 cm DW 
or larger occur most commonly at depths of 400 m-600 m (Arkhipkin et 
al. 2008). Despite these depth changes, studies around the Falkland 
Islands have shown little evidence of large spatial or temporal 
movements, which could indicate that graytail skates carry out their 
entire life cycle within the waters where they hatch (Agnew et al. 
2000; Wakeford et al. 2005; Winter et al. unpublished).
    Range-wide abundance estimates for graytail skate are not 
available; however, biomass estimates exist for the populations off the 
Falkland Islands and Argentina. In the Falkland Islands, graytail skate 
were part of the fish assemblage of both the southern and northern 
skate and ray stocks. They were particularly abundant south of the 
islands, making them dominant in catches of the southern skate and ray 
assemblage. However, due to declining CPUEs of the southern stock, 
especially for graytail skate, the southern rajid fishery was closed in 
1996 (Agnew et al. 1999; Agnew et al. 2000; Wakeford et al. 2005). 
Current biomass estimates from this area could not be found. North of

[[Page 76107]]

the Falkland Islands, declines in the CPUE of graytail skate were also 
observed between 1992 and 2001 (Wakeford et al. 2005); however, based 
on recent biomass estimates, the population appears to have recovered 
and stabilized. Specifically, analysis of 2010 fishery survey cruise 
data resulted in an estimated biomass of graytail skate of 7,232 t, 
which is consistent with the earlier biomass estimates for the species 
from the 1990s (Falkland Islands Government 2011). As this biomass 
estimate is just for the graytail skate population north of the 
Falkland Islands, it is likely a significant underestimation of the 
total biomass for the entire Falkland Islands population, especially 
considering the southern stock, which was historically more abundant, 
has been protected from targeted fishing since 1996.
    In 2002, S[aacute]nchez and Mabraga[ntilde]a (2002) estimated the 
population abundance of the graytail skate on the continental Argentine 
shelf between 48[deg] S. and 55[deg] S. to be 259,210 individuals, or 
2,431.98 t. This estimate was calculated prior to the apparent recovery 
of the graytail skate in the Falkland Islands and also corresponds to 
when CPUE of the graytail skate was at its minimum in the Falkland 
Islands (Wakeford et al. 2005). As such, it could be assumed that 
biomass has since increased on the shelf; however, with no recent 
abundance estimates available, the trends within this portion of the 
species' range cannot be determined with certainty.
    Farther north on the Argentine shelf, between 45[deg] S. and 
41[deg] S., the biomass of graytail skate was estimated to be 503 t in 
2004, but had a large confidence interval (2,237 
t), with an average density of the species of 0.05 t/nm\2\ (Colonello 
and Massa 2004). More recent estimates or trends in population 
abundance or biomass levels for graytail skate are not available.
    There is very little information pertaining to the presence of 
graytail skate in Uruguayan and Chilean waters. No information on 
commercial, recreational, or research catches of graytail skate is 
available from Uruguay. Likewise, there is no estimate of abundance 
from this area. In Chile, graytail skate are found south of 41[deg] S. 
and at depths of 137 m to 595 m (McCormack et al. 2007). In 1995, Saez 
and Lamilla (2004) caught 42 graytail skate between March and December 
at 350 m depth approximately 20 miles from Punta Galera; however, no 
other information is available on scientific or commercial catch 
distribution or population abundance from this area.

Summary of Factors Affecting the Graytail Skate

    We reviewed the best available information regarding historical, 
current, and potential threats to the graytail skate species. We find 
that the main threat to this species is overutilization for commercial 
purposes; however, we consider the severity of this threat to be 
greatly reduced by the regulatory mechanisms in place in the Falkland 
Islands, where the species was historically most heavily exploited. 
Thus, we find that historical and present levels of utilization are not 
exceeding the species' biological capacity to sustain current levels of 
exploitation. We also find that current regulatory measures are 
adequate to protect the species from further overutilization. 
Additionally, available information does not indicate that habitat 
destruction or modification, disease, predation or other natural or 
manmade factors are operative threats on these species. We summarize 
information regarding these factors and their interactions below 
according to section 4(a)(1) of the ESA. See Casselbury and Carlson 
(2015g) for a more detailed discussion of these factors.

Present or Threatened Destruction, Modification, or Curtailment of 
Habitat or Range

    Trawl fisheries occur throughout the graytail skate's range. 
Studies show that the interaction of bottom trawling gears with bottom 
substrate can have negative effects on benthic fish habitat 
(Valdemarsen et al. 2007). These impacts are often the most serious on 
hard substrates with organisms that grow up from the bottom, such as 
corals and sponges, but alterations to soft substrates have also been 
seen. The trawl doors on bottom otter trawls often cause the most 
damage to the ocean bottom, but other parts of trawling gear, such as 
weights, sweeps, and bridles that contact the bottom can also be 
damaging. Intense fishing disturbance from trawling has reduced the 
abundance of several benthic species (Valdemarsen et al. 2007); 
however, there is no specific information available that indicates this 
habitat modification has had a direct effect on the abundance of the 
graytail skate, or is specifically responsible for the curtailment of 
its habitat or range.

Overutilization for Commercial, Recreational, Scientific, or 
Educational Purposes

    Information available on the harvest of the graytail skate 
indicates that they are most heavily exploited in the Falkland Islands 
multispecies skate and ray fishery by foreign fleets (Agnew et al. 
1999; Falkland Islands Government 2005-2013). Prior to the 1990s, 
catches from the Falkland Islands were mainly attributed to Spanish 
vessels fishing in a mixed groundfish fishery, with rajid catches of 
less than 1,500 t per year (Wakeford et al. 2005). However, in 1989, 
Korean vessels began to specifically target rajids in this fishery 
using demersal trawls, and by 1991 catches of skates and rays rose to 
more than 7,000 t/year (Wakeford et al. 2005). Subsequently, two rather 
distinct rajid fisheries developed within the Falkland Islands: a 
southern rajid fishery that fished in a small area south of the 
Falkland Islands (a ray ``hot spot;'' Agnew et al. 2000), and a 
northern rajid fishery that operated in a more extensive area to the 
north of the Falkland Islands (primarily on the slope between 200 m-400 
m depths; Wakeford et al. 2005). In the 1990s, the graytail skate was 
the most important species caught in the Falkland Islands multispecies 
rajid fisheries based on catch weight, and was estimated to make up 
approximately 58 percent of the catch in the southern rajid fishery and 
39 percent of the catch in the northern rajid fishery between 1993 and 
1995 (Agnew et al. 1999; Bizikov et al. 2004). However, with this heavy 
exploitation on the skate populations by Korean fleets (which were 
responsible for 88 percent of the directed rajid catch between 1990 and 
1997; Agnew et al. 2000), the proportional catches of graytail skate 
declined in all areas that were fished. This decline was particularly 
precipitous in the southern batoid aggregation area, where graytail 
skate spawn (A. Winter, pers. comm. 2015) and had previously comprised 
the majority of the catch (Agnew et al. 1999). Agnew et al. (2000) 
calculated that total mortality rates (fishing mortality rates + 
natural mortality rates) in the northern and southern areas were 
significantly higher than what could be sustained by the batoid 
assemblage, particularly graytail skates. Specifically, the authors 
estimated that graytail skates could sustain total mortality rates of 
less than 0.3/year; however, the total mortality rate in the northern 
area from 1991-1995 was on the order of 0.42/year and in the southern 
area was 0.61/year (Agnew et al. 2000). Consequently, significant 
declines in CPUE were observed between 1990 and 1997. A steep 58 
percent decline was noted in the southern rajid fishery from 1993 to 
1996, which was attributed to the decline in graytail skate abundance

[[Page 76108]]

(Agnew et al. 1999, 2000) and declines ranging from 44 to 65 percent 
were observed for the northern rajid fishery from 1990-1996 (Agnew et 
al. 2000). For catches of graytail skate, Wakeford et al. (2005) 
estimated a decline in CPUE of around 70 percent between 1992 and 2001 
in the northern rajid fishery, and observer data indicate CPUE of 
graytail skate continued to decline through 2007 (Winter et al. 
unpublished). Catches of graytail skate also showed a reduction in 
average disc width. From 1993-1995, average disc width declined from 
52.18 cm to 31.91 cm (Agnew et al. 2000), and based on observer data 
collected from the Falkland Islands Inner Conservation and Management 
Zone (located between 49[deg] S.-54[deg] S. and 64[deg] W.-54[deg] W.), 
the majority of graytail skate catches in the commercial trawl fishery 
from 1997-2006 were still relatively small skates with modal disc 
widths between 25 cm and 40 cm (Arkhipkin et al. 2008). Additionally, 
about 54 percent of the catches were female skates with disc widths 
between 10 cm and 80 cm, and the majority were under the estimated size 
at 50 percent maturity (Arkhipkin et al. 2008).
    As a result of the marked declines in CPUE, particularly for the 
entire southern batoid aggregation, which was presumed to be driven by 
declines in graytail skate (Agnew et al. 1999, 2000; Wakeford et al. 
2005), the southern ray fishery was closed in 1996 and separate skate 
target trawling licenses and catch limits (of around 3,000 t through 
the late 1990s) were imposed in the northern ray fishery. Following the 
implementation of these catch limits, which equated to between 6.5 and 
7.6 percent of the estimated pre-exploitation biomass, the northern 
rajid stock appeared to stabilize by 2000 (Agnew et al. 2000). In fact, 
based on a stock assessment of the northern skate stock, with updated 
data through 2014, estimated biomass of the entire stock has gradually 
and consistently increased since 1996, from a low of 13,641 t in 1989 
(95 percent CI: 10,591-24,214), which marked the start of heavy 
exploitation, to a recent peak high of 34,558 t in 2014 (90 percent CI: 
27,284-59,806) (Fisheries Committee 2015). In addition, CPUE of the 
northern stock has been gradually increasing over the years (Agnew et 
al. 2000; Falkland Islands Fisheries Committee 2015) whereas targeting 
of skate and ray species in the Falkland Islands has been decreasing, 
with a large portion (almost half) of the skate catch now taken as 
bycatch under finfish licenses (Falkland Islands Government 2014). In 
fact, the most recent data from the fishery show that in 2014 total 
skate catch amounted to 5,543.2 t, with 53 percent of this total 
representing targeted skate catch (Fisheries Committee 2015). 
Furthermore, even with the proportional increase in bycaught skates and 
decrease in targeted skate catch, the total skate catch for the fishery 
appears sustainable as it falls below the Maximum Sustainable Yield 
(MSY) estimate, which is the theoretical largest catch that can be 
taken from a stock. Based on the latest stock assessment of the 
northern skate assemblage, MSY is estimated to be 6,048 t (95 percent 
CI: 6,198-46,811), which is approximately 8 percent higher than the 
2014 total skate catch (Fisheries Committee 2015).
    In terms of the graytail skate, despite the reported historical 
reductions in CPUE, B. griseocauda remains one of the most abundant 
species caught in the Falkland Islands multispecies skate fishery 
(Agnew et al. 1999; Arkhipkin et al. 2008; Falkland Islands Government 
2005, 2006, 2007, 2008, 2010, 2011, 2012) and presently makes up 
between 11 percent and 18 percent of the skate trawl catch and bycatch 
identified by observers (Agnew et al. 2000; Falkland Islands Government 
2010, 2011, 2012, 2014). Recent data from the Falkland Islands 
Government (2012) also indicate that the modal disc width of graytail 
skate catches has increased to 63 cm in 2012. The increase in modal 
disc width could be indicative of population recovery for graytail 
skates in recent years. This is supported by the fact that in 2010, 
fishery-independent surveys conducted to estimate skate biomass in the 
northern area of the Falkland Islands (the area that generally yields 
the highest skate catches by the targeted skate fishery) confirm that 
total skate biomass, and particularly the predominant skate species, 
including graytail skate, have remained stable in recent years. Using 
CPUE as an index of abundance, an analysis incorporating more recent 
data from 1994 to 2013 revealed that B. griseocauda was in decline 
until about 2007, with a decrease in CPUE from 120.1 kg/hr in 1994 to 
22.6 kg/hr in 2007 (Winter et al. unpublished). However, CPUE has since 
increased to an estimated 70.1 kg/hr in 2013, similar to levels 
observed in 1997-2001, with abundance continuing on a positive trend 
(Winter et al. unpublished). Furthermore, given that these estimates 
are only for graytail skate in the northern area of the Falkland 
Islands, it is likely that the total abundance of the Falkland Islands 
population is significantly higher and has recovered even more so due 
to the complete ban on commercial skate fishing in the southern batoid 
aggregation area, where the spawning grounds of the species are mostly 
located (A. Winter, pers. comm. 2015).
    Given the evidence of increasing CPUE and biomass of the northern 
skate assemblage, skate catch estimates that are below MSY, stable 
biomass estimates of graytail skate, and increasing abundance and sizes 
of graytail skates in catches, the current fishing effort and level of 
exploitation of skates in general, and graytail skate in particular, in 
the Falkland Islands appears to be sustainable (Falkland Islands 
Government 2014). In other words, overutilization of the species in 
this portion of its range is not a threat that is contributing 
significantly to its risk of extinction.
    In Argentina, an active commercial elasmobranch fishery, which 
exploits sharks, skates, and rays, has shown an increasing trend in 
both catches and number of vessels reporting skate and ray landings 
since the early 1990s. Historically, skates and rays were mainly 
discarded as fisheries bycatch, but are now landed as both target and 
non-target catch (Chiaramonte 1998; Massa and Hozbor 2003). 
Specifically, catches have increased from 183 t in 1991 to 13,265 t in 
2000, and vessels reporting landings have increased from 69 in 1992 to 
377 in 1998 (S[aacute]nchez and Mabraga[ntilde]a 2002; Massa and Hozbor 
2003). From 1994-1998, Massa and Hozbor (2003) estimated a decline of 
around 36 percent in the CPUE of large fishing vessels (>28 m in 
length) for all skates and rays on the Argentine shelf between 34 and 
48[deg] S.; however, the data are not species-specific and deep-water 
skates, like the graytail skate, are generally not monitored despite 
the fact that they are under fishing pressure (Massa et al. 2004b). 
Additionally, the CPUE of skates and rays for smaller fishing vessels 
(with lengths <28 m) did not show similar declines; rather, CPUE for 
these vessels on the Argentine shelf remained fairly stable from 1994-
1998 (Massa and Hozbor 2003).
    Along the Patagonian shelf, the graytail skate has also been 
observed as bycatch in the scallop (Zygochlamys patagonica) fishery. 
This Patagonian scallop fishery primarily operates along the 100 m 
isobath, between 36[deg]43' S and 48[deg]30' S, and uses non-selective 
bottom otter trawls (Schejter et al. 2012). In a research study 
examining the bycatch composition from this fishery, the graytail skate 
occurred in 6.8 percent of the sampled fishing sites (n=177) (Schejter 
et al. 2012); however, no information on abundance of the species 
within those sites was provided. Overall, the limited abundance data as

[[Page 76109]]

well as the lack of species-specific information and trends data makes 
it difficult to determine the magnitude of utilization that may be 
occurring specifically for B. griseocauda in this part of its 
Argentinian range, and whether this level of utilization is 
contributing significantly to the species' extinction risk.
    Similarly, little information is available on the exploitation of 
the graytail skate in Chilean waters. There is a directed skate fishery 
off Chile that primarily targets the yellownose skate (Zearaja 
chilensis), and although information on the depth at which the fishery 
operates could not be found, Z. chilensis lives at depths between 28 m 
and 435 m. This depth range overlaps with the shallower half of the 
graytail skate's depth range (Kyne et al. 2007) and thus this fishery 
may also incidentally catch graytail skates. Since 1979, declines in Z. 
chilensis catches have been reported, and it is suspected that other 
skate species, including the graytail skate, have also been affected 
(McCormack et al. 2007); however, graytail skate comprise less than 5 
percent of the skate landings in this fishery (McCormack et al. 2007). 
As such, the impact of this fishery on graytail skate abundance and 
overall extinction risk is likely to be minimal.

Disease or Predation

    At this time, there is no available information regarding diseases 
or predators of the species. As such, there is no evidence to indicate 
that these factors are a threat to the graytail skate.

Inadequacy of Existing Regulatory Mechanisms

    In the Falkland Islands, there are numerous management measures in 
place that provide for the protection of graytail skate from 
overutilization. The Falkland Islands multispecies fishery, where 
graytail skate is presumably most heavily exploited, is rigorously 
managed through fishing effort controls. In order to protect the 
southern batoid aggregation area that displayed marked declines in CPUE 
in the early 1990s (Agnew et al. 1999), the Falkland Islands government 
implemented a number of management measures to ensure long-term 
sustainability of the rajid fishery, including: (1) The placement of 
observers on vessels to identify batoids to species and collect other 
biological data to inform fisheries management; (2) the development of 
specific skate and ray fishery seasons and licenses to better regulate 
the catch of rajids; and (3) the implementation and continuation of a 
prohibition on trawling for skates and rays south of 51[deg] S, which 
effectively closed the southern ray fishery. Before the prohibition, 
graytail skate were particularly abundant south of the islands, where 
its spawning grounds are mostly located (A. Winter, pers. comm. 2015), 
and made up a significant portion of the catch from this area. Thus, 
this measure helps protect not only a large segment of the population 
from further depletion in an area where they were historically most 
concentrated, but also important life history behavior required for the 
survival of the species (Agnew et al. 2000). In addition to the closure 
of the southern ray fishery via the trawl prohibition, catch limits 
were also imposed for the northern rajid fishery in 1996. Since then, 
the northern batoid stock has seen a gradual increase in both CPUE and 
biomass, with total catches lower than MSY, suggesting regulatory 
measures are adequate in providing for the sustainable exploitation of 
the northern skate assemblage in Falkland waters. Data also suggest 
that these regulatory measures have allowed for the recovery of the 
graytail skate population, as indicated by the increasing CPUE and 
sizes of graytail skate in recent catches. As such, the Fisheries 
Committee, which advises the Falkland Islands Fisheries Department, 
recommended maintaining the skate target catch at the current level of 
effort allocation for the 2016 fishing year as these limits are 
effective at maintaining a sustainable multispecies fishery and appear 
adequate to protect the graytail skate from extinction.
    In Argentina, the graytail skate is covered under the country's FAO 
NPOA-sharks; however, it is not considered a priority species. Several 
sources have noted that Argentina does little to actively protect 
elasmobranchs, particularly skates and rays, in its waters (Massa and 
Hozbor 2003; Massa et al. 2004b, McCormack et al. 2007). Though total 
allowable catch, minimum sizes, and annual quotas are in place for many 
elasmobranchs in Argentina, they are largely ignored and poorly 
enforced (McCormack et al. 2007). In 2013, El Instituto Nacional de 
Investigaci[oacute]n y Desarrollo Pesquero (INIDEP) set the recommended 
total allowable catch for all skates and rays at 9,000 t and a landing 
limit for skates and rays was set at no more than 30 percent of the 
catch. However, due to the lack of information regarding the status of 
the graytail skate in Argentina, there is no indication that existing 
regulatory mechanisms are inadequate in controlling threats to the 
species or are contributing significantly to the species' risk of 
extinction.
    In Uruguay, the graytail skate is considered a species of high 
priority under Uruguay's FAO NPOA-sharks, which outlines plans to: 
investigate the species' age, growth, reproduction, diet, distribution, 
and habitat use in Uruguayan waters; generate a time series for catch 
and effort of the skate in fisheries; conduct an abundance assessment; 
establish measures to review current fishing licenses for graytail 
skate and determine possible modifications to the licenses; and 
finally, prohibit new fishing permits. However, aside from the species' 
presence in Uruguayan waters, there is a significant lack of 
information regarding the status of graytail skate in Uruguay; thus, 
there is no indication that existing regulatory mechanisms are 
inadequate in controlling threats to the species in this portion of its 
range, or are contributing significantly to its risk of extinction.
    In Chile, there are little to no regulations for the protection of 
graytail skate; however, the exploitation of the species in Chilean 
waters is minimal. While there are regulations pertaining to other 
fisheries in Chilean waters that overlap the graytail skate's range, it 
is unknown how these regulations affect the status of graytail skate. 
Based on the available information, there is no indication that 
existing regulatory mechanisms are inadequate in controlling threats to 
the species in this portion of its range, or are contributing 
significantly to its risk of extinction.

Other Natural or Manmade Factors Affecting the Species

    Besides the information already discussed above in the other factor 
sections, no additional information was found regarding threats to the 
species that would fall under this category. As such, there is no 
evidence to indicate that this factor is a threat to the graytail 
skate.

Extinction Risk

Demographic Risk Analysis

Abundance
    Although range-wide abundance estimates for graytail skate are 
unavailable; biomass estimates and trends exist for the areas where the 
species was historically and is currently most abundant. In the 
Falkland Islands, graytail skate represented a dominant part of the 
southern rajid assemblage in the mid-1990s and comprised around 39 
percent of the northern rajid catch. Due to heavy fishing pressure 
contributing to unsustainable mortality rates, significant declines in 
the CPUE of the species were observed between 1992 and 2007 indicating 
a likely reduction in population abundance. However,

[[Page 76110]]

since the decline, CPUE (as an index of abundance of graytail skate) 
from north of the Falkland Islands has been increasing, already 
reaching levels observed in 1997-2001, with biomass of the species in 
2010 estimated to be 7,232 t, consistent with biomass estimates from 
the early 1990s. Additionally, the graytail skate remains one of the 
most abundant species caught in the Falkland Islands multispecies skate 
fishery. Therefore, while the species likely experienced historical 
declines in abundance as a result of heavy exploitation in the early 
1990s, the available information on biomass estimates and trends 
between the 1990s and 2014 indicate that the population is potentially 
stabilized and even recovering. Therefore, the species' present level 
of abundance is unlikely to pose a demographic risk to the species. 
Furthermore, there is no other abundance information or trend data from 
the rest of the species' range to indicate that the species' present 
abundance level is contributing significantly to its risk of 
extinction.
Growth Rate/Productivity
    Relative growth rates (k) of graytail skates were estimated to be 
0.064 year-1 in Argentinean waters (i.e., low), and 0.02 
year-1 to 0.033 year-1 in the Falkland Islands 
(i.e., very low). Graytail skates are long-lived species, with an 
estimated lifespan of approximately 28 years, and a maximum disc width 
of 130 cm. Although age and growth studies from skates in the same 
region provide conflicting estimates for length and age at maturity, 
with age of maturity estimates ranging from 14-17.6 years for males and 
17.8-24.8 years for females, all estimates indicate a very late age of 
maturity. While there is some evidence to suggest that graytail skates 
may reproduce year-round, overall, these reproductive characteristics 
suggest the species has relatively low productivity, similar to other 
elasmobranch species, which may hinder its ability to quickly rebound 
from threats that decrease its abundance (such as overutilization) and 
render the species more vulnerable to extinction in the face of other 
demographic risks and threats. Additionally, the observed decrease in 
the species' mean disc width in catches from 1993-1995 and 1997-2006 
(to sizes that ranged between 25 cm and 40 cm) likely portended a 
declining growth rate for the species. This is because changes in 
metrics, such as average size, can significantly impact other important 
life history functions, like fecundity or even natural mortality rates 
(Audzijonyte et al. 2015), that affect the instantaneous per capita 
growth rate of a species. However, since 2006, data from the Falkland 
Islands Government show an increase in size of the modal disc width of 
graytail skate catches, with the most recent size estimate of 63 cm in 
2012, likely indicating that the population is recovering and that 
growth rate is no longer declining.
Spatial Structure/Connectivity
    Based on trends in commercial fisheries data from the Falkland 
Islands and Argentina, Wakeford et al. (2005) concluded that graytail 
skates have limited spatial and temporal movements and, therefore, may 
likely exist as localized populations. Limited inter-population 
exchange reduces the recovery potential for depleted and small local 
populations and may increase the risk of local extirpations, possibly 
leading to complete extinction. However, no other information is 
available regarding spatial structure or connectivity of graytail skate 
populations throughout its range, and there is no evidence to suggest 
this demographic risk is presently significantly contributing to the 
graytail skate's risk of extinction.
Diversity
    The loss of diversity can increase a species' extinction risk 
through decreasing a species' capability of responding to episodic or 
changing environmental conditions. This can occur through a significant 
change or loss of variation in life history characteristics (such as 
reproductive fitness and fecundity), morphology, behavior, or other 
genetic characteristics. Currently, there is no information regarding 
the graytail skates' diversity throughout its range, thus we can not 
conclude whether its present level of diversity is contributing to its 
extinction risk.

Threats Assessment

    The best available information indicates that graytail skates are 
most heavily exploited in the Falkland Islands multispecies skate and 
ray fishery by foreign fleets and likely suffered significant declines 
in abundance due to overexploitation in the early 1990s. However, since 
1996, the area of operation of the Falkland Islands rajid fishery has 
been significantly restricted (to an area north of the Islands) with 
imposed catch limits to manage the northern batoid stock assemblage 
(which includes graytail skates) within this area. As a result of these 
management measures, there has been a gradual increase in CPUE and 
biomass of the northern batoid stock assemblage. As for graytail skates 
specifically, they remain one of the most abundant species caught in 
the Falkland Islands multispecies skate fishery. Recent data from the 
Falkland Islands Government shows an increasing trend in the CPUE of 
the species as well as in the the modal disc width of graytail skate 
catches, with the latest estimate of 63 cm DW in 2012. While 63 cm is 
still below the size of sexual maturity (i.e., 75 cm) it is a marked 
improvement from the modal disc widths between 1993 and 2006 (after 
heavy exploitation), which ranged between 25 cm and 40 cm, and 
indicates potential recovery of the population. Additionally, since the 
early 2000s, there has been a general decreasing trend in the targeting 
of skate and ray species in the Falkland Islands, with most species now 
taken as bycatch in the finfish fishery. Furthermore, total skate catch 
in recent years has remained below MSY, indicating that current catch 
and effort of the skate and ray fishery are likely sustainable. Based 
on the above information, it is clear that existing regulatory 
measures, including current catch limits and trawling closures, are 
adequate to protect the graytail skate in the Falkland Islands from 
extinction.
    In Argentina, there is an active commercial elasmobranch fishery, 
which exploits sharks, skates, and rays, and it has shown an increasing 
trend in both catches and number of vessels reporting skate and ray 
landings (Massa and Hozbor 2003). However, based on the lack of 
species-specific information from the region, it is highly uncertain if 
present levels of utilization of skates and rays are a threat that is 
contributing significantly to the extinction risk of the graytail 
skate.
    In Chile, a directed skate fishery that primarily targets Zearaja 
chilensis in areas where graytail skate may also occur has reported 
declines in catch since 1979. It is suspected that other skate species, 
including the graytail skate, have also been affected. However, there 
are no available data that indicate a decline in graytail skate 
abundance or catch, and given that the species comprises less than 5 
percent of the total skate landings in this fishery, it is unlikely 
that this fishery is significantly contributing to the extinction risk 
of the graytail skate.
    Overall, while the species likely experienced historical declines 
in abundance during the 1990s due to exploitation by the Falkland 
Islands multispecies rajid fisheries, the available biomass estimates 
and trends over the past decade, including gradual increases in the 
CPUE and biomass of

[[Page 76111]]

the northern batoid stock and specifically the graytail skate in recent 
years, as well as an increasing trend in graytail modal disc width 
size, indicate the population is potentially stable and possibly moving 
towards recovery. This is likely a result of rigorous regulations 
implemented by the Falkland Islands government to sustainably manage 
the rajid fishery by reducing fishing effort, accomplished by setting 
catch limits in the northern rajid fishery and closing the southern 
rajid fishery area, where graytail skates likely spawn and were 
historically most heavily exploited. It should be noted that while this 
closure helps to protect the Falkland Islands population, due to 
uncertainty surrounding the connectivity of graytail skate populations, 
these regulations may not provide protection to skate populations found 
outside of Falkland waters. However, based on the available 
information, it appears that the Falkland Islands is where the species 
is most concentrated, and, hence, the protection of this population 
from extinction is likely critical for the survival of the species. 
Outside of the Falkland Islands, the minimal available information on 
the species does not indicate that present levels of utilization or any 
other factors are contributing significantly to the extinction risk of 
the species.

Risk of Extinction

    While the species' demographic characteristics increase its 
inherent vulnerability to depletion, and likely contributed to past 
population declines of varying magnitudes, the best available 
information suggests these risks have decreased due to the adequate 
control of exploitation of the species. In the Falkland Islands, where 
the species was most heavily exploited and is likely presently most 
concentrated, abundance estimates and trends from the 1990s to 2013, 
and increases in the species' mean disc width, suggest potential 
stabilization and even recovery of the population. The continued 
rigorous management and monitoring of the fishery appears adequate in 
protecting the species from levels of overutilization that would 
increase its extinction risk. Despite fishing pressure in other parts 
of the species' range (e.g., Chile and Argentina) and evidence of it 
being taken as bycatch in various fisheries, graytail skates are not 
monitored and we have no other information (e.g., catch rates, 
abundance trends, or any other species-specific data) to indicate that 
present levels of utilization or any other factors are significantly 
contributing to the species' risk of extinction. Thus, considering the 
above information and analysis, we conclude that B. griseocauda is at a 
low risk of extinction throughout its range, and as such, does not 
warrant listing as a threatened or endangered species throughout its 
range.

Significant Portion of Its Range Analysis

    Because our range-wide analysis for the species leads us to 
conclude that the species is not threatened or endangered throughout 
its range, under the final Significant Portion of Its Range (SPR) 
policy announced in July 2014, we must go on to consider whether the 
species may have a higher risk of extinction in a significant portion 
of its range (79 FR 37577; July 1, 2014).
    The final policy explains that it is necessary to fully evaluate a 
portion for potential listing under the ``significant portion of its 
range'' authority only if information indicates that the members of the 
species in a particular area are likely both to meet the test for 
biological significance and to be currently endangered or threatened in 
that area. Making this preliminary determination triggers a need for 
further review, but does not prejudge whether the portion actually 
meets these standards such that the species should be listed:
    To identify only those portions that warrant further consideration, 
we will determine whether there is substantial information indicating 
that (1) the portions may be significant and (2) the species may be in 
danger of extinction in those portions or likely to become so within 
the foreseeable future. We emphasize that answering these questions in 
the affirmative is not a determination that the species is endangered 
or threatened throughout a significant portion of its range--rather, it 
is a step in determining whether a more detailed analysis of the issue 
is required (79 FR 37586, July 1, 2014).
    Thus, the preliminary determination that a portion may be both 
significant and endangered or threatened merely requires NMFS to engage 
in a more detailed analysis to determine whether the standards are 
actually met (Id. at 37587). Unless both are met, listing is not 
warranted. The policy further explains that, depending on the 
particular facts of each situation, NMFS may find it is more efficient 
to address the significance issue first, but in other cases it will 
make more sense to examine the status of the species in the potentially 
significant portions first. Whichever question is asked first, an 
affirmative answer is required to proceed to the second question. Id. 
(``[I]f we determine that a portion of the range is not 
``significant,'' we will not need to determine whether the species is 
endangered or threatened there; if we determine that the species is not 
endangered or threatened in a portion of its range, we will not need to 
determine if that portion was ``significant.''). Thus, if the answer to 
the first question is negative--whether that regards the significance 
question or the status question--then the analysis concludes and 
listing is not warranted.
    After a review of the best available information, we identified the 
Falkland Islands as likely constituting a ``significant'' portion of 
the graytail skate range. Under the policy, a portion of a species' 
range is significant if, without that portion, the species would have 
an increased vulnerability to threats to the point that the overall 
species would be in danger of extinction or likely to become so in the 
foreseeable future. As mentioned previously, the historical and current 
fisheries data indicate that graytail skate are likely most 
concentrated in Falkland waters. Graytail skate have also been 
identified and caught elsewhere throughout its range, such as north of 
the Falkland Islands on the Argentinian shelf between 45[deg] S. and 
41[deg] S., and on the Pacific coast off Chile (south of 41[deg] S.); 
however, based on trends in commercial fisheries data from the Falkland 
Islands and Argentina, Wakeford et al. (2005) concluded that graytail 
skates have limited spatial and temporal movements and, therefore, may 
likely exist as localized or isolated populations. If we assume the 
Falkland Islands population is isolated from the populations of 
graytail skate elsewhere throughout its range, then, technically, loss 
of this population would not directly affect the abundance of the other 
remaining populations. However, loss of this population could 
significantly increase the extinction risk of the species as a whole, 
as only small, fragmented, and isolated populations of the species 
(based on the best available abundance information--see the Historical 
and Current Distribution and Population Abundance and Demographic Risk 
Analysis sections above) would remain, making them more vulnerable to 
catastrophic events and environmental or anthropogenic perturbations. 
Limited inter-population exchange also reduces the recovery potential 
for these small local populations and increases the risk of local 
extirpations and overall complete extinction.
    Under the policy, if we believe the Falkland Islands population may 
constitute a ``significant'' portion of the range, then we must either 
evaluate the extinction risk of this population first to determine 
whether it is threatened or endangered in that portion or determine

[[Page 76112]]

if this portion is, in fact, ``significant.'' Ultimately, of course, 
both tests have to be met to qualify the species for listing. Given the 
extremely limited amount of information on the species outside of its 
Falkland Islands range, it is difficult to conduct a more definitive 
analysis to determine whether or not this portion does, in fact, 
constitute a ``significant'' portion of the range of the graytail 
skate. Additionally, there is no information to suggest that any other 
portion may be significant. However, even if we were to assume that the 
Falklands Islands population does constitute a ``significant'' portion 
of the graytail skate range, based on the information and analysis in 
the previous extinction risk section, there are no identified threats 
concentrated in this portion that are significantly contributing to the 
species' risk of extinction. In fact, the most recent available 
information indicate that existing regulatory measures are adequate in 
protecting the graytail skate in the Falkland Islands from extinction, 
with graytail skate abundance on a positive trend and exhibiting signs 
of population recovery based on both CPUE and size data. Thus, under 
the policy, the preliminary determination that a portion of the 
species' range may be both significant and endangered or threatened has 
not been met. Therefore, listing is not warranted under the SPR policy.

Proposed Determination

    Based on the best available scientific and commercial information 
as presented in the status review report and this finding, we find that 
the graytail skate is not presently in danger of extinction throughout 
all or a significant portion of its range, nor is it likely to become 
so in the foreseeable future. We summarize the factors supporting this 
conclusion as follows: (1) Although there is no formal estimate of the 
current population size and historical declines in biomass have been 
observed, current biomass estimates from the Falkland Islands, where 
the species is likely most concentrated, suggest the population is 
stable and CPUE trends indicate abundance is increasing; (2) a 
reduction in mean disc width of the Falkland Islands population 
occurred in the late 1990s and early 2000s as a result of intensive 
fishing pressure; however, recent evidence suggests an increase in 
modal disc width, which is likely indicative of population recovery; 
(3) while an identified threat to the species was historical 
overutilization in the Falkland Islands commercial fisheries, 
subsequent fishery closures in the southern rajid fishery and catch 
limits in the northern rajid fishery of the Falkland Islands have 
contributed to a significant reduction of fishing pressure on the 
species, leading to increases in the abundance of the population and 
providing for sustainable fishing of the northern Falkland Islands 
rajid assemblage; (4) targeting of skates and rays in the Falkland 
Islands, where the species was most heavily exploited, has been on a 
decreasing trend since the early 2000s; (5) there is no evidence that 
destruction of habitat, disease or predation are factors contributing 
to an increased risk of extinction for the species; and (6) the 
continual implementation of rigorous monitoring and fishery management 
measures in the Falkland Islands appears effective in addressing the 
most important threat to the species (overharvest) now and into the 
foreseeable future. Based on these findings, we conclude that the 
graytail skate is not presently in danger of extinction throughout all 
or a significant portion of its range, nor is it likely to become so 
within the foreseeable future. Accordingly, the graytail skate does not 
meet the definition of a threatened or endangered species and therefore 
does not warrant listing as threatened or endangered at this time.

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 for endangered species (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 the proposed 
endangered listings are prohibitions on take, including export and 
import.

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 the listing of these species under 
the ESA will increase the number of section 7 consultations, because 
these species occur outside of the United States and are unlikely to be 
affected by Federal actions.

Critical Habitat

    Critical habitat is defined in section 3 of the ESA (16 U.S.C. 
1532(5)) as: (1) The specific areas within the geographical area 
occupied by a species, at the time it is listed in accordance with the 
ESA, on which are found those physical or biological features (a) 
essential to the conservation of the species and (b) that may require 
special management considerations or protection; and (2) specific areas 
outside the geographical area occupied by a species at the time it is 
listed upon a determination that such areas are essential for the 
conservation of the species. ``Conservation'' means the use of all 
methods and procedures needed to bring the species to the point at 
which listing under the ESA is no longer necessary. 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)).
    The best available scientific and commercial data as discussed 
above identify the geographical areas occupied by Isogomphodon 
oxyrhynchus, Rhinobatos horkelii, Mustelus fasciatus, M. schmitti, 
Squatina guggenheim and S. argentina as being entirely outside U.S. 
jurisdiction, so we cannot designate critical habitat for these 
species.
    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 on 
these species does not indicate that U.S. waters provide any

[[Page 76113]]

specific essential biological function for any of the species proposed 
for listing. Therefore, based on the available information, we do not 
intend to designate critical habitat for Isogomphodon oxyrhynchus, 
Rhinobatos horkelii, Mustelus fasciatus, M. schmitti, Squatina 
guggenheim or S. argentina.

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 Isogomphodon oxyrhynchus, 
Rhinobatos horkelii, Mustelus fasciatus and Squatina argentina as 
endangered, all of the prohibitions of section 9(a)(1) of the ESA will 
apply to these species. These include prohibitions on 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 these 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 these species or any part of these 
species.
    We emphasize that whether a violation results from a particular 
activity is entirely dependent upon the facts and circumstances of each 
incident. Further, an activity not listed may in fact constitute a 
violation.

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 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;
    (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).

Protective Regulations Under Section 4(d) of the ESA

    We are proposing to list Mustelus fasciatus and Squatina guggenheim 
as 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. We will 
consider extending some or all potential protective regulations 
pursuant to section 4(d) for the proposed threatened species. We seek 
public comment on potential 4(d) protective regulations (see below).

Public Comments Solicited

    To ensure that any final action resulting from this proposed rule 
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 any of the six species 
proposed for listing;
    (2) Taxonomic information on any of these species;
    (3) Biological information (life history, genetics, population 
connectivity, etc.) on any of these species;
    (4) Efforts being made to protect any of these species throughout 
their current ranges;
    (5) Information on the commercial trade of any of these species;
    (6) Historical and current distribution and abundance and trends 
for any of these species;
    (7) Current or planned activities within the range of these species 
and their possible impact on these species; and,
    (8) Information relevant to potential ESA section 4(d) protective 
regulations for any of the proposed threatened 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 peer review comments on the species' status review reports 
(Casselbury and Carlson 2015a-

[[Page 76114]]

g) from 22 scientists from the academic and scientific community that 
were either familiar with the species or had expertise in elasmobranch 
biology, ecology, or conservation. We received comments from nine 
scientists and incorporated those comments into the status review 
reports and this proposed rule. Their comments on the status reviews 
are also summarized in the peer review report available at http://www.cio.noaa.gov/services_programs/prplans/PRsummaries.html.

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), we have 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 the species occurs, 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 all 
three species. As the process continues, we intend to continue engaging 
in informal and formal contacts with 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, Imports, 
Transportation.

50 CFR Part 224

    Endangered and threatened species, Exports, Imports, 
Transportation.

    Dated: November 30, 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

0
1. The authority citation for part 223 continues to read as follows:

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

0
2. In Sec.  223.102, amend the table in paragraph (e) by adding new 
entries for two species in alphabetical order under the ``Fishes'' 
table subheading to read as follows:


Sec.  223.102  Enumeration of threatened marine and anadromous species.

* * * * *
    (e) * * *

----------------------------------------------------------------------------------------------------------------
                            Species \1\
--------------------------------------------------------------------  Citation(s) for     Critical
                                                    Description of        listing         habitat     ESA rules
          Common name            Scientific name     listed entity    determination(s)
----------------------------------------------------------------------------------------------------------------
 
                                                  * * * * * * *
----------------------------------------------------------------------------------------------------------------
                                                     Fishes
----------------------------------------------------------------------------------------------------------------
 
                                                  * * * * * * *
Shark, spiny angel............  Squatina           Entire species..  Federal Register            NA           NA
                                 guggenheim.                          citation and
                                                                      date when
                                                                      published as a
                                                                      final rule.
Shark, narrownose smoothhound.  Mustelus schmitti  Entire species..  Federal Register            NA           NA
                                                                      citation and
                                                                      date when
                                                                      published as a
                                                                      final rule.
 
                                                  * * * * * * *
----------------------------------------------------------------------------------------------------------------
\1\ Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement,
  see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56
  FR 58612, November 20, 1991).
\2\ Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration,
  National Marine Fisheries Service, is limited to turtles while in the water.
 [79 FR 20806, Apr. 14, 2014, as amended at 79 FR 38240, July 3, 2014; 79 FR 40015, July 11, 2014; 79 FR 54122,
  Sept. 10, 2014; 80 FR 7978, Feb. 13, 2015]


[[Page 76115]]

PART 224--ENDANGERED MARINE AND ANADROMOUS SPECIES

0
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.

0
4. In Sec.  224.101, paragraph (h), amend the table by adding new 
entries for four species in alphabetical order under the ``Fishes'' 
table subheading to read as follows:


Sec.  224.101  Enumeration of endangered marine and anadromous species.

* * * * *
    (h) * * *

----------------------------------------------------------------------------------------------------------------
                            Species \1\
--------------------------------------------------------------------  Citation(s) for     Critical
                                                    Description of        listing         habitat     ESA rules
          Common name            Scientific name     listed entity    determination(s)
----------------------------------------------------------------------------------------------------------------
 
                                                  * * * * * * *
----------------------------------------------------------------------------------------------------------------
                                                     Fishes
----------------------------------------------------------------------------------------------------------------
 
                                                  * * * * * * *
Guitarfish, Brazilian.........  Rhinobatos         Entire species..  Federal Register            NA           NA
                                 horkelii.                            citation and
                                                                      date when
                                                                      published as a
                                                                      final rule.
Shark, Argentine angel........  Squatina           Entire species..  Federal Register            NA           NA
                                 argentina.                           citation and
                                                                      date when
                                                                      published as a
                                                                      final rule.
Shark, daggernose.............  Isogomphodon       Entire species..  Federal Register            NA           NA
                                 oxyrhynchus.                         citation and
                                                                      date when
                                                                      published as a
                                                                      final rule.
Shark, striped smoothhound....  Mustelus           Entire species..  Federal Register            NA           NA
                                 fasciatus.                           citation and
                                                                      date when
                                                                      published as a
                                                                      final rule.
 
                                                  * * * * * * *
----------------------------------------------------------------------------------------------------------------
\1\ Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement,
  see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56
  FR 58612, November 20, 1991).
\2\ Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration,
  National Marine Fisheries Service, is limited to turtles while in the water.
 [79 FR 20814, Apr. 14, 2014, as amended at 79 FR 31227, June 2, 2014; 79 FR 38241, July 3, 2014; 79 FR 74005,
  Dec. 12, 2014; 79 FR 78725, Dec. 31, 2014; 79 FR 68372, Nov. 17, 2014; 80 FR 7978, Feb. 13, 2015; 80 FR 7390,
  Feb. 10, 2015]

[FR Doc. 2015-30660 Filed 12-4-15; 8:45 am]
 BILLING CODE 3510-22-P