Endangered and Threatened Wildlife and Plants; 12-Month Finding for 7 Foreign Species of Elasmobranchs Under the Endangered Species Act, 76067-76115 [2015-30660]
Download as PDF
Vol. 80
Monday,
No. 234
December 7, 2015
Part II
Department of Commerce
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
PO 00000
Frm 00001
Fmt 4717
Sfmt 4717
E:\FR\FM\07DEP2.SGM
07DEP2
76068
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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
National Marine Fisheries
Service (NMFS), National Oceanic and
Atmospheric Administration (NOAA),
Commerce.
ACTION: Proposed rule; 12-month
petition finding; request for comments.
AGENCY:
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.
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
SUMMARY:
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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-20150161. 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 https://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:
DATES:
DEPARTMENT OF COMMERCE
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
PO 00000
Frm 00002
Fmt 4701
Sfmt 4702
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
https://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
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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 https://
www.nmfs.noaa.gov/pr/species/
petition81.htm or on the respective
species pages found on the Office of
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
Protected Resources Web site (https://
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 https://
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 12month 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 https://
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
PO 00000
Frm 00003
Fmt 4701
Sfmt 4702
76069
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,
E:\FR\FM\07DEP2.SGM
07DEP2
76070
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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).
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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
´
´
˜
Amapa, Para, and Maranhao, with
˜
˜
Tubarao Bay in Maranhao 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 °C
to 31.5 °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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 Marajo 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
PO 00000
Frm 00004
Fmt 4701
Sfmt 4702
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
´
Cortes (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
(m1) 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 Cortes (2002), which means
this species generally has a low
potential to recover from exploitation.
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
Historical and Current Distribution and
Population Abundance
In Brazil, daggernose sharks were
historically found in the states of
´
´
˜
Amapa, Para, and Maranhao, and were
first formally recorded in surveys from
˜
the 1960s in the state of Maranhao
(Lessa 1986). In 1999, daggernose sharks
were documented as occurring in two
Marine Conservation Areas in northern
Brazil, the Parque Nacional Cabo Orange
´
ˆ
in Amapa, and the Reentrancias
˜
Maranhenses in Maranhao (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
Braganca fish market in northern Brazil
¸
´
(State of Para), 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
˜
Maranhao 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
´
Cervigon 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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 Para, 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 Maranhao coast,
harvest of daggernose sharks would
begin in October and peak in January,
with the catch per unit effort (CPUE) of
PO 00000
Frm 00005
Fmt 4701
Sfmt 4702
76071
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
´
˜
Para (Lessa et al. 2010) or Maranhao
(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
´
´
Amapa and Para), 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 Maranhao 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;
´
Ministerio 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
´
(Ministerio do Meio Ambiente/Instituto
Brasileiro do Meio Ambiente e dos
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
76072
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
´
Recursos Naturais Renovaveis (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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 Especies da Fauna
Ameacadas de Extincao—Peixes e
¸
¸˜
´
Invertebrados Aquaticos’’ (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
ˆ
Orange and the Reentrancias
Maranhenses (Lessa et al. 1999b);
PO 00000
Frm 00006
Fmt 4701
Sfmt 4702
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
˜
Maranhao, 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
ˆ
of the Reentrancias 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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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 5year 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.
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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)
PO 00000
Frm 00007
Fmt 4701
Sfmt 4702
76073
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
E:\FR\FM\07DEP2.SGM
07DEP2
76074
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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 Para,
and was caught in large numbers by the
artisanal gillnet fisheries operating on
˜
the Maranhao 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
´
´
Amapa and Para) and Northwest region
˜
(which includes the States of Maranhao
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.
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00008
Fmt 4701
Sfmt 4702
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
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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 °C, while in the summer, individuals
are found in average water temperatures
of 26 °C (Lessa and Vooren 2005).
Brazilian guitarfish are commonly found
in salinities ranging from 24–28 ppt in
northern Argentina (Jaureguizar et al.
2006).
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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° and 34° 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°36′ S.) to Arroio Chuı
(33°45′ S.). In historical bottom trawl
surveys between latitudes 28°00′ S. and
34°30′ S., R. horkelii was common
across the Plataforma Sul south of
latitude 29°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 Chuı and Solidao (Rio Grande
do Sul, Brazil) in February 2005 found
an average CPUE of 1.68 kg/hr (Vooren
PO 00000
Frm 00009
Fmt 4701
Sfmt 4702
76075
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° S.–43° S.), estimated
mean biomass of Brazilian guitarfish
was 0.1240 t/nm2 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/
nm2 in 1981. Estimated biomass then
peaked at 0.441 t/nm2 in 1994 before
falling steadily to 0.007 t/nm2 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.
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
76076
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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° S.–34° 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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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° S.–30° 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
PO 00000
Frm 00010
Fmt 4701
Sfmt 4702
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 Sao
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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 Gestao 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
PO 00000
Frm 00011
Fmt 4701
Sfmt 4702
76077
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 Sao 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 Cananeia´
˜
Iguape-Peruıbe (Sao Paulo; 234,000
hectares), PARNA do Superagui (Parana;
33,988 hectares), REBIO do Arvoredo
(Santa Catarina; 17,600 hectares) and
´
RESEX Marinha do Pirjubae (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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
76078
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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 fisheryrelated 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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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.
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.
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.
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.
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° S. and 34° S.
in southern Brazil, and it is scarce
elsewhere. On the northern Argentine
continental shelf, between 34° S. and
43° 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/nm2. Biomass
peaked in 1994 at 0.441 t/nm2 before
falling to 0.007 t/nm2 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,
PO 00000
Frm 00012
Fmt 4701
Sfmt 4702
Spatial Structure/Connectivity
The species is thought to have a
continuous distribution along the
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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.
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 bycatchrelated 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° S. and 34° 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° S.–30° 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
PO 00000
Frm 00013
Fmt 4701
Sfmt 4702
76079
population from fishing pressure are no
longer protected from exploitation.
˜
In July 2010, the State of Sao 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).
E:\FR\FM\07DEP2.SGM
07DEP2
76080
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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.
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 greybrown 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 Bahıa
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
´
Chuı 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).
PO 00000
Frm 00014
Fmt 4701
Sfmt 4702
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 Chuı 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 °C–15 °C
for juveniles during winter months, and
>16 °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
˜
Solidao 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
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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.
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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 Bahıa Blanca in
Buenos Aires Province, Argentina.
While striped smoothhound were once
considered a dominant permanent
resident in Rio Grande do Sul in the
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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).
PO 00000
Frm 00015
Fmt 4701
Sfmt 4702
76081
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 Mendonca 1996; Vooren
¸
and Klippel 2005b). Striped
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
76082
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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 Chuı 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
km2. 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 Chuı 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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 km2 occupied area, in
depths between 2 m–5 m: An area of
only 395 km2. 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 Mendonca 1996; Vooren
¸
and Klippel 2005b). As such, all lifestages 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
PO 00000
Frm 00016
Fmt 4701
Sfmt 4702
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 (Direccion Nacional de
´
Recursos Acuaticos (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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
(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 NPOAsharks, 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° S. and 34° 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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00017
Fmt 4701
Sfmt 4702
76083
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
E:\FR\FM\07DEP2.SGM
07DEP2
76084
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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.
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 NPOAsharks, 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
PO 00000
Frm 00018
Fmt 4701
Sfmt 4702
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
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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)
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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° S. and 47°45′ S. (Belleggia
et al. 2012). Rio de Janeiro, Brazil, is the
northernmost limit of the species’ range
´
(Oddone et al. 2007) and Rıa 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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
smoothhound is found in waters with
surface temperatures of 8 °C–11.7 °C
and bottom temperatures of 5.5 °C–11 °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 °C and
20 °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
´
´
Rıo de la Plata and El Rincon,
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,
PO 00000
Frm 00019
Fmt 4701
Sfmt 4702
76085
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 yolksac viviparous (Hamlett et al. 2005;
´
Galındez 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 midDecember 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; Galındez et al. 2010). Litter
size increases significantly with
maternal length (Oddone et al. 2005;
´
Cortes 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 Rincon area
´
(including Bahıa Blanca and Anegada
´
Bay) and the Rıo de la Plata (including
´
Samborombon Bay) (Chiaramonte and
Pettovello 2000; Molina and Cazorla
2011).
E:\FR\FM\07DEP2.SGM
07DEP2
76086
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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 Rıo 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).
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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, Cortes (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, Cortes (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 (Cortes 2007). These demographic
parameters place narrownose
smoothhound toward the faster growing
end of the ‘‘fast-slow’’ continuum of
population parameters calculated by
´
Cortes (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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
off Rio de la Plata as high as 44 t/nm2
in 1994 (Cousseau et al. 1998).
Throughout the rest of the ArgentineUruguayan 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/nm2, with some areas supporting
densities as high as 22 t/nm2 (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° S.–41° 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°
S.–48° 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°
S.–41° 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
PO 00000
Frm 00020
Fmt 4701
Sfmt 4702
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 (Galındez 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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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° S. and 41° 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 (Cortes
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
year-round in the surrounding El
´
Rincon 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
´
Rincon 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 Rincon 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
´
Rincon 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
´
Rincon 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
PO 00000
Frm 00021
Fmt 4701
Sfmt 4702
76087
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,
´
Cortes (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,
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
76088
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 Lamonaca
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, Rıa Deseado (∼40 km; 47°45′
S.; 65°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 Rıa Deseado waters in the late
spring and stay until late summer
(Chiaramonte and Pettovello 2000).
Anegada Bay (39°50′51″ S. to 40°43′08″
S. and 62°28′44″ W. to 62°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,
PO 00000
Frm 00022
Fmt 4701
Sfmt 4702
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 Rincon 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 fisheryrelated 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 Comision Tecnica Mixta del Frente
´
Marıtimo (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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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/nm2; 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° 5/11, Res. N° 5/02), and
in 2012, the CTMFM set a speciesspecific total permissible catch limit for
narrownose smoothhound at 4,500 t
(Res. N° 11/13, Res. N° 9/12). This catch
limit remained at this level until 2015,
when it was reduced to 3,500 t (Res N°
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° 445). As described in
previous species assessments, an Annex
1 listing prohibits the catch of the
species except for scientific purposes,
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00023
Fmt 4701
Sfmt 4702
76089
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°
S.–41° 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
E:\FR\FM\07DEP2.SGM
07DEP2
76090
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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 (Cortes 2007). These
estimates indicate that M. schmitti has
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00024
Fmt 4701
Sfmt 4702
comprises a single demographic unit in
´
the Rıo de la Plata area and its maritime
front (area separating Uruguay and
Argentina), with no distinct population
structure found between or within the
´
Rıo 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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 speciesspecific 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,
PO 00000
Frm 00025
Fmt 4701
Sfmt 4702
76091
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; Cortes 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
E:\FR\FM\07DEP2.SGM
07DEP2
76092
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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.
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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; Schafer 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
PO 00000
Frm 00026
Fmt 4701
Sfmt 4702
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
´
Espırito Santo, Brazil, to Rawson,
¨
Argentina (Milessi et al. 2001; Vogler 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 °C
and 22 °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 (Vogler et al.
¨
2003; Colonello 2005; Vogler 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
¨
(Vogler et al. 2003). Crustaceans (4.8
percent), molluscs (4.4 percent), and
polychaetes (0.46 percent) made up the
¨
remaining portions (Vogler 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 (Vogler et
al. 2003, 2009).
Although ontogenetic and seasonal
differences in diet have been observed
¨
for the species (Vogler et al. 2003;
¨
Colonello 2005; Vogler et al. 2009),
bony fish remain the primary prey item
for all size classes and during all
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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
¨
(Vogler 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).
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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 Matıas 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 Rincon,
Argentina, found that males from El
´
Rincon at a given length were
significantly heavier than males from
Rio de la Plata, while females showed
no significant differences in the lengthweight relationship (Colonello et al.
2007). Both sexes grew larger in El
´
Rincon than in Rio de la Plata
(Colonello et al. 2007); but, length at 50
percent maturity in males was not
significantly different between El
´
Rincon 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 Rincon (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∞) of 94.7
cm TL. Length and age at first maturity
is estimated to be 72 cm TL and 4 years,
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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°50′ S. and 33°30′ S. at
depths less than 20 m is considered a
nursery area for spiny angel sharks
(Vooren and Klippel 2005a).
PO 00000
Frm 00027
Fmt 4701
Sfmt 4702
76093
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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
76094
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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 °C and
¨
above 20 °C (Vogler et al. 2008).
¨
Specifically, Vogler et al. (2008) found
that spiny angel sharks concentrate in
water temperatures between 13.2 °C and
18.5 °C in the spring and between 7.0
°C and 15.0 °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 (Vogler 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 Solidao to Chuı,
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, Sao Paulo, Brazil caught spiny
angel sharks in shallow sampling
stations around 20 m deep, but found
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 Matıas Gulf,
Argentina (southern Argentina) was
estimated to be 192.53 t (Argentina FAO
NPOA-sharks 2009); however, the San
´
Matıas 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° S.
and 41° 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/nm2 in 1981, 1.305 t/nm2 in
1995, and 0.394 t/nm2 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/km2 (equivalent to
2.58–5.15 t/nm2) (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
PO 00000
Frm 00028
Fmt 4701
Sfmt 4702
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° S. and 28° 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
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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 Matıas
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; Vogler 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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00029
Fmt 4701
Sfmt 4702
76095
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 (Vogler 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; Vogler 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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
76096
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00030
Fmt 4701
Sfmt 4702
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
´
Chuı, 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 km2, 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 km2 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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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 atvessel 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 atvessel 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.
VerDate Sep<11>2014
19:37 Dec 04, 2015
Jkt 238001
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° 8/14, Res. N° 10/
13, Res. N° 10/12). In November 2012,
this limit was met and landings of
Squatina spp. were banned for the
month of December (Res. N° 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° 10/13, Res. N° 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° 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 fisheryrelated 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
PO 00000
Frm 00031
Fmt 4701
Sfmt 4702
76097
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 yearround (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° 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 NPOAsharks and would benefit from the
proposed fishing closures and other
E:\FR\FM\07DEP2.SGM
07DEP2
76098
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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 Matıas 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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00032
Fmt 4701
Sfmt 4702
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
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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.
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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 biparentallyinherited 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). Fisheryindependent research surveys have
recorded relatively high densities of the
species on the Argentinian shelf;
however, based on CPUE data, the
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 (Vogler 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 NPOAsharks. 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; Vogler 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
PO 00000
Frm 00033
Fmt 4701
Sfmt 4702
76099
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 fisheryrelated 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
E:\FR\FM\07DEP2.SGM
07DEP2
76100
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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).
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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.
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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).
PO 00000
Frm 00034
Fmt 4701
Sfmt 4702
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
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
population increase of the Argentine
angel shark is currently unknown.
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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/nm2) along the Uruguayan
coast in the AUCFZ, where salinities are
´
higher than the Argentine coast (Dıaz 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 Chuı 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 °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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00035
Fmt 4701
Sfmt 4702
76101
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
´
Chuı 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° S.–34° 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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
76102
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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° S. to 34° 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 Chuı (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 Lamonaca
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
PO 00000
Frm 00036
Fmt 4701
Sfmt 4702
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
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 NPOAsharks; 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°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 bycatchrelated mortality in the fishery.
Overall, regulatory mechanisms for
the monkfish fishery, particularly the
ban of chartered foreign gillnets from
21° S. to the southern extent of Brazil’s
PO 00000
Frm 00037
Fmt 4701
Sfmt 4702
76103
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 Chuı in Rio
Grande do Sul, with no evidence of
abundant populations outside this
region. Based on fishery-independent
E:\FR\FM\07DEP2.SGM
07DEP2
76104
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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,
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00038
Fmt 4701
Sfmt 4702
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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00039
Fmt 4701
Sfmt 4702
76105
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 (Saez and Lamilla
2004). They have been caught at
latitudes as far north as 39° S. in the
Pacific Ocean and 34° S. in the Atlantic
Ocean, and as far south as 60° S. in the
Southern Ocean on the Antarctic shelf
(Bigelow and Schroeder 1965; Figueroa
´
et al. 1999; Saez 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
E:\FR\FM\07DEP2.SGM
07DEP2
76106
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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 (Sanchez and Mabragana 2002). Off
the coast of Argentina, the graytail skate
´
did not consume crustaceans (Sanchez
˜
and Mabragana 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, Bucker (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∞) 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∞) 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∞) 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
´
˜
(Sanchez and Mabragana 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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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° 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; Bucker
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° S. and in the southeastern Pacific
Ocean, south of 39° S. (Figueroa et al.
´
1999; Saez 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° S. and
41° S. respectively (McCormack et al.
2007), where they exhibit strict
PO 00000
Frm 00040
Fmt 4701
Sfmt 4702
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 °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
¨
(Bucker 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° S. and 41° 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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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, Sanchez and Mabragana
(2002) estimated the population
abundance of the graytail skate on the
continental Argentine shelf between 48°
S. and 55° 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° S. and 41° 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/nm2
(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° 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.
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00041
Fmt 4701
Sfmt 4702
76107
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
E:\FR\FM\07DEP2.SGM
07DEP2
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
76108
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
(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°
S.–54° S. and 64° W.–54° 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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00042
Fmt 4701
Sfmt 4702
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 (Sanchez and
˜
Mabragana 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° S.; however, the
data are not species-specific and deepwater 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°43′ S and
48°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
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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.
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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°
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 Investigacion 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
PO 00000
Frm 00043
Fmt 4701
Sfmt 4702
76109
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,
E:\FR\FM\07DEP2.SGM
07DEP2
76110
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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 interpopulation 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
PO 00000
Frm 00044
Fmt 4701
Sfmt 4702
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
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00045
Fmt 4701
Sfmt 4702
76111
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° S. and 41° S., and on the
Pacific coast off Chile (south of 41° 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
E:\FR\FM\07DEP2.SGM
07DEP2
76112
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00046
Fmt 4701
Sfmt 4702
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
E:\FR\FM\07DEP2.SGM
07DEP2
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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.
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
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.
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
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
PO 00000
Frm 00047
Fmt 4701
Sfmt 4702
76113
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–
E:\FR\FM\07DEP2.SGM
07DEP2
76114
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
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 https://
www.cio.noaa.gov/services_programs/
prplans/PRsummaries.html.
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.
References
A complete list of the references used
in this proposed rule is available upon
request (see ADDRESSES).
Executive Order 13132, Federalism
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,
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.
Species 1
Common name
*
Scientific name
*
Description of listed entity
*
*
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
1. The authority citation for part 223
continues to read as follows:
■
Authority: 16 U.S.C. 1531–1543; subpart
B, § 223.201–202 also issued under 16 U.S.C.
1361 et seq.; 16 U.S.C. 5503(d) for
§ 223.206(d)(9).
2. In § 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:
■
§ 223.102 Enumeration of threatened
marine and anadromous species.
*
*
*
(e) * * *
*
Citation(s) for listing
determination(s)
*
*
Critical
habitat
*
ESA rules
*
Fishes
*
Shark, spiny angel .............
*
*
Squatina guggenheim .......
*
Entire species ...................
Shark, narrownose
smoothhound.
Mustelus schmitti ..............
Entire species ...................
*
*
*
*
*
*
Federal Register citation
and date when published as a final rule.
Federal Register citation
and date when published as a final rule.
*
*
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
1 Species
*
NA
NA
NA
NA
*
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]
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
PO 00000
Frm 00048
Fmt 4701
Sfmt 4702
E:\FR\FM\07DEP2.SGM
07DEP2
76115
Federal Register / Vol. 80, No. 234 / Monday, December 7, 2015 / Proposed Rules
PART 224—ENDANGERED MARINE
AND ANADROMOUS SPECIES
Authority: 16 U.S.C. 1531–1543 and 16
U.S.C 1361 et seq.
‘‘Fishes’’ table subheading to read as
follows:
3. The authority citation for part 224
continues to read as follows:
■
4. In § 224.101, paragraph (h), amend
the table by adding new entries for four
species in alphabetical order under the
§ 224.101 Enumeration of endangered
marine and anadromous species.
■
Species 1
Common name
*
Scientific name
*
Description of listed entity
*
*
*
*
*
(h) * * *
*
Citation(s) for listing
determination(s)
*
*
Critical
habitat
*
ESA rules
*
Fishes
*
Guitarfish, Brazilian ............
*
*
Rhinobatos horkelii ...........
*
Entire species ...................
Shark, Argentine angel ......
Squatina argentina ............
Entire species ...................
Shark, daggernose ............
Isogomphodon
oxyrhynchus.
Entire species ...................
Shark, striped
smoothhound.
Mustelus fasciatus ............
Entire species ...................
*
*
*
*
*
*
Federal Register citation
and date when published as a final rule.
Federal Register citation
and date when published as a final rule.
Federal Register citation
and date when published as a final rule.
Federal Register citation
and date when published as a final rule.
*
*
1 Species
*
NA
NA
NA
NA
NA
NA
NA
NA
*
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]
mstockstill on DSK4VPTVN1PROD with PROPOSALS2
BILLING CODE 3510–22–P
VerDate Sep<11>2014
18:45 Dec 04, 2015
Jkt 238001
PO 00000
Frm 00049
Fmt 4701
Sfmt 9990
E:\FR\FM\07DEP2.SGM
07DEP2
Agencies
[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
https://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 https://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 https://www.nmfs.noaa.gov/pr/species/petition81.htm or on the respective species pages found on the Office
of Protected Resources Web site (https://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 https://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 https://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