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

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DEPARTMENT OF COMMERCE DATES: Comments on this proposed rule addresses the findings for 7 of those 27 must be received by February 5, 2016. species: daggernose shark National Oceanic and Atmospheric Public hearing requests must be made (Isogomphodon oxyrhynchus), Brazilian Administration by January 21, 2016. guitarfish (Rhinobatos horkelii), striped ADDRESSES: You may submit comments smoothhound shark (Mustelus 50 CFR Parts 223 and 224 on this document, identified by NOAA– fasciatus), narrownose smoothhound [Docket No. 150909839–5839–01] NMFS–2015–0161, by either of the shark (Mustelus schmitti), spiny angel following methods: shark (Squatina guggenheim), Argentine RIN 0648–XE184 • Electronic Submissions: Submit all angel shark (Squatina argentina), and electronic public comments via the graytail skate (Bathyraja griseocauda). Endangered and Threatened Wildlife Federal eRulemaking Portal. Go to The status of, and relevant Federal and Plants; 12-Month Finding for 7 www.regulations.gov/ Register notices for, the other 20 species Foreign Species of Elasmobranchs #!docketDetail;D=NOAA-NMFS-2015- can be found on our Web site at Under the Endangered Species Act 0161. Click the ‘‘Comment Now’’ icon, http://www.nmfs.noaa.gov/pr/species/ petition81.htm. AGENCY: National Marine Fisheries complete the required fields, and enter We are responsible for determining Service (NMFS), National Oceanic and or attach your comments. • whether species are threatened or Atmospheric Administration (NOAA), Mail: Submit written comments to endangered under the ESA (16 U.S.C. Commerce. NMFS Office of Protected Resources (F/ PR3), 1315 East West Highway, Silver 1531 et seq.). To make this ACTION: Proposed rule; 12-month Spring, MD 20910, USA. determination, we consider first petition finding; request for comments. Instructions: Comments sent by any whether a group of organisms constitutes a ‘‘species’’ under the ESA, SUMMARY: We, NMFS, have completed other method, to any other address or then whether the status of the species comprehensive status reviews under the individual, or received after the end of qualifies it for listing as either Endangered Species Act (ESA) for seven the comment period, may not be threatened or endangered. Section 3 of foreign marine elasmobranch species in considered by NMFS. All comments the ESA defines a ‘‘species’’ to include response to a petition to list those received are a part of the public record ‘‘any subspecies of fish or wildlife or species. These seven species are the and will generally be posted for public viewing on www.regulations.gov plants, and any distinct population daggernose shark (Isogomphodon segment of any species of vertebrate fish oxyrhynchus), Brazilian guitarfish without change. All personally identifying information (e.g., name, or wildlife which interbreeds when (Rhinobatos horkelii), striped mature.’’ On February 7, 1996, NMFS smoothhound shark (Mustelus address, etc.), confidential business information, or otherwise sensitive and the U.S. Fish and Wildlife Service fasciatus), narrownose smoothhound (USFWS; together, the Services) adopted shark (Mustelus schmitti), spiny angel information submitted voluntarily by the sender will be publicly accessible. a policy describing what constitutes a shark (Squatina guggenheim), Argentine distinct population segment (DPS) of a angel shark (Squatina argentina), and NMFS will accept anonymous comments (enter ‘‘N/A’’ in the required taxonomic species (the DPS Policy; 61 graytail skate (Bathyraja griseocauda). FR 4722). The DPS Policy identified two Based on the best scientific and fields if you wish to remain anonymous). elements that must be considered when commercial information available, and identifying a DPS: (1) The discreteness You can find the petition, status review after taking into account efforts being of the population segment in relation to report, Federal Register notices, and the made to protect these species, we have the remainder of the species (or determined that the daggernose shark (I. list of references electronically on our subspecies) to which it belongs; and (2) oxyrhynchus), Brazilian guitarfish (R. Web site at http://www.nmfs.noaa.gov/ the significance of the population horkelii), striped smoothhound shark pr/species/petition81.htm. segment to the remainder of the species (Mustelus fasciatus), and Argentine FOR FURTHER INFORMATION CONTACT: (or subspecies) to which it belongs. As angel shark (S. argentina) meet the Maggie Miller, NMFS, Office of stated in the DPS Policy, Congress definition of an endangered species Protected Resources (OPR), (301) 427– expressed its expectation that the under the ESA. We have determined 8403 or Chelsey Young, NMFS, OPR, Services would exercise authority with that the narrownose smoothhound shark (301) 427–8491. regard to DPSs sparingly and only when (M. schmitti) and spiny angel shark (S. SUPPLEMENTARY INFORMATION: the biological evidence indicates such guggenheim) meet the definition of a Background action is warranted. Based on the threatened species under the ESA. scientific information available we Therefore, we propose to list these six On July 15, 2013, we received a determined that the daggernose shark (I. species under the ESA. Additionally, we petition from WildEarth Guardians to oxyrhynchus), Brazilian guitarfish (R. have determined that the graytail skate list 81 marine species as threatened or horkelii), striped smoothhound shark (B. griseocauda) does not warrant listing endangered under the Endangered (M. fasciatus), narrownose under the ESA at this time. We are not Species Act (ESA). This petition smoothhound shark (M. schmitti), spiny proposing to designate critical habitat included species from many different angel shark (S. guggenheim), Argentine for any of the species proposed for taxonomic groups, and we prepared our angel shark (S. argentina), and graytail listing because the geographical areas 90-day findings in batches by taxonomic skate (B. griseocauda) are ‘‘species’’ occupied by these species are entirely group. We found that the petitioned under the ESA. There is nothing in the outside U.S. jurisdiction, and we have actions may be warranted for 27 of the scientific literature indicating that any not identified any unoccupied areas 81 species and announced the initiation of these species should be further within U.S. jurisdiction that are of status reviews for each of the 27 divided into subspecies or DPSs. currently essential to the conservation species (78 FR 63941, October 25, 2013; Section 3 of the ESA defines an of any of these species. We are soliciting 78 FR 66675, November 6, 2013; 78 FR endangered species as ‘‘any species comments on our proposal to list these 69376, November 19, 2013; 79 FR 9880, which is in danger of extinction six foreign marine elasmobranch February 21, 2014; and 79 FR 10104, throughout all or a significant portion of species. February 24, 2014). This document its range’’ and a threatened species as

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one ‘‘which is likely to become an Protected Resources Web site (http:// level according to four demographic endangered species within the www.nmfs.noaa.gov/pr/species/ viability factors: Abundance, growth foreseeable future throughout all or a index.htm). These status reviews rate/productivity, spatial structure/ significant portion of its range.’’ We compiled information on each species’ connectivity, and diversity. These interpret an ‘‘endangered species’’ to be biology, ecology, life history, and threats viability factors reflect concepts that are one that is presently in danger of from information contained in the well-founded in conservation biology extinction. A ‘‘threatened species,’’ on petition, our files, a comprehensive and that individually and collectively the other hand, is not presently in literature search, and consultation with provide strong indicators of extinction danger of extinction, but is likely to experts. The draft status review reports risk. become so in the foreseeable future (that (Casselberry and Carlson 2015 a–g) were In conducting the threats assessment, is, at a later time). In other words, the submitted to independent peer we identified and summarized the primary statutory difference between a reviewers and comments and section 4(a)(1) factors that are currently threatened and endangered species is information received from peer operating on the species and their likely the timing of when a species may be in reviewers were addressed and impact on the biological status of the danger of extinction, either presently incorporated as appropriate before species. We also looked for future (endangered) or in the foreseeable future finalizing the draft report. The peer threats (where the impact on the species (threatened). review report is available at http:// has yet to be manifested) and When we consider whether a species www.cio.noaa.gov/services_programs/ considered the reliability to which we might qualify as threatened under the prplans/PRsummaries.html. These could forecast the effects of these threats ESA, we must consider the meaning of status reviews did not include and future events on the status of these the term ‘‘foreseeable future.’’ It is extinction risk analyses for the species; species. appropriate to interpret ‘‘foreseeable thus, the extinction risk analyses for the Using the findings from the future’’ as the horizon over which seven species are included in this 12- demographic risk analysis and threats predictions about the conservation month finding. In addition to the status assessment, we evaluated the overall status of the species can be reasonably review reports, we considered extinction risk of the species. Because relied upon. The foreseeable future information submitted by the public in species-specific information (such as considers the life history of the species, response to our petition finding as well current abundance) is sparse, qualitative habitat characteristics, availability of as information we compiled to assess ‘‘reference levels’’ of risk were used to data, particular threats, ability to predict the extinction risk of the species to describe extinction risk. The definitions threats, and the reliability to forecast the make our determinations. of the qualitative ‘‘reference levels’’ of effects of these threats and future events extinction risk were as follows: ‘‘Low on the status of the species under Extinction Risk Analyses Risk’’—a species is at a low risk of consideration. Because a species may be We considered the best available extinction if it exhibits a trajectory susceptible to a variety of threats for information and applied professional indicating that it is unlikely to be at a which different data are available, or judgment in evaluating the level of risk moderate level of extinction risk in the which operate across different time faced by each of the seven species. For foreseeable future (see description of scales, the foreseeable future is not each extinction risk analysis, we ‘‘Moderate Risk’’ below). A species may necessarily reducible to a particular evaluated the species’ demographic be at low risk of extinction due to its number of years. risks (demographic risk analysis), such present demographics (i.e., stable or Section 4(a)(1) of the ESA requires us as low abundance and productivity, and increasing trends in abundance/ to determine whether any species is threats to the species including those population growth, spatial structure and endangered or threatened due to any of related to the factors specified by the connectivity, and/or diversity) with the following factors: the present or ESA section 4(a)(1)(A)–(E) (threats projected threats likely to have threatened destruction, modification, or assessment), and then synthesized this insignificant impacts on these curtailment of its habitat or range; information to estimate the extinction demographic trends; ‘‘Moderate Risk’’— overutilization for commercial, risk of the species (risk of extinction). a species is at moderate risk of recreational, scientific, or educational The demographic risk analysis, extinction if it exhibits a trajectory purposes; disease or predation; the mentioned above, is an assessment of indicating that it will more likely than inadequacy of existing regulatory the manifestation of past threats that not be at a high level of extinction risk mechanisms; or other natural or have contributed to the species’ current in the foreseeable future (see description manmade factors affecting its continued status and informs the consideration of of ‘‘High Risk’’ below). A species may be existence. Under section (4)(b)(1)(A), we the biological response of the species to at moderate risk of extinction due to its are also required to make listing present and future threats. For this present demographics (i.e., declining determinations based solely on the best analysis, we considered the trends in abundance/population growth, scientific and commercial data demographic viability factors developed spatial structure and connectivity, and/ available, after conducting a review of by McElhany et al. (2000). The approach or diversity and resilience) and/or the species’ status and after taking into of considering demographic risk factors projected threats and its likely response account efforts being made by any state to help frame the consideration of to those threats; ‘‘High Risk’’—a species or foreign nation to protect the species. extinction risk has been used in many is at high risk of extinction when it is of our status reviews, including for at or near a level of abundance, spatial Status Reviews Pacific salmonids, Pacific hake, walleye structure and connectivity, and/or Status reviews for the petitioned pollock, Pacific cod, Puget Sound diversity that place its persistence in species addressed in this finding were rockfishes, Pacific herring, scalloped question. The demographics of the conducted by a contractor for the NMFS and great hammerhead sharks, and species may be strongly influenced by Southeast Fisheries Science Center and black abalone (see http:// stochastic or depensatory processes. are available at http:// www.nmfs.noaa.gov/pr/species/ for Similarly, a species may be at high risk www.nmfs.noaa.gov/pr/species/ links to these reviews). In this approach, of extinction if it faces clear and present petition81.htm or on the respective the collective condition of individual threats (e.g., confinement to a small species pages found on the Office of populations is considered at the species geographic area; imminent destruction,

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modification, or curtailment of its capture of daggernose sharks in shallow takes place at the end of the dry season habitat; or disease epidemic) that are waters during the rainy season when or at the beginning of the rainy season likely to create such imminent waters are less saline (Lessa 1997). (Barthem 1985). The gestation period is demographic risks. Specific winter habitats of the approximately 12 months, with a Below we summarize information daggernose shark are unknown. protracted birthing period throughout from the status review reports and Diet and Feeding the 6-month rainy season (Lessa et al. information we compiled on the seven 1999a; Lessa et al. 2006b). Mature Little is known about the diet and foreign marine elasmobranch species, females captured with flaccid uteri and feeding of the daggernose shark. analyze extinction risk of each species, white follicles indicate that there is a assess protective efforts to determine if Bigelow and Schroeder (1948) and Compagno (1984) suggest that they feed break in follicle development between they are adequate to mitigate existing two successive pregnancies, which threats to each species, and propose on schooling fishes, such as clupeids, indicates a 2-year reproductive cycle determinations based on the status of sciaenids, herring, anchovies, and (Lessa et al. 1999a). Mating and each of the seven foreign marine croakers. It is speculated that their small elasmobranch species. eyes and elongated snout emphasize the gestation periods can also be postponed use of their rostral sense organs over to compensate for climate variability Daggernose Shark (Isogomphodon eyesight when hunting in turbid waters and changing environmental conditions oxyrhynchus) (Compagno 1984). In Marajo´ Bay in across years (Lessa et al. 1999a). Female Species Description Brazil, daggernose sharks were found fecundity is low, commonly ranging eating catfish (Family Ariidae) (Barthem between 3 to 7 embryos per female, with The daggernose shark (Isogomphodon 1985). the largest litter observed containing 7 oxyrhynchus) is the only species in the embryos, and one report of a female genus Isogomphodon, in the family Growth and Reproduction with 8 embryos (Bigelow and Schroeder Carcharhinidae (Compagno 1988). It has Growth rates of daggernose sharks are 1948; Barthem 1985; Lessa et al. 1999a). a uniform gray or gray-brown color and similar between males and females, There is no significant relationship white underside (Compagno 1984; with an estimated growth rate from birth Compagno 1988; Grace 2001), and is to age 1 calculated to be approximately between female size and litter size in identified by its prominent, elongated 14 cm/year (Lessa et al. 2000). This rate daggernose sharks (Lessa et al. 1999a). snout. The pectoral fins of the species then slows to approximately 10 cm/year Genetics and Population Structure are very large and paddle-shaped from age 1 to 5–6 for males and age 1 (Compagno 1984; Compagno 1988; to 6–7 for females (Lessa et al. 2000). Studies examining the genetics of the Grace 2001). Thus, estimated ages at maturity are 5– species or information on its population 6 years for males and 6–7 years for Range and Habitat Use structure could not be found. females. In terms of size, male The daggernose shark occurs in the daggernose sharks begin maturing Demography central western Atlantic Ocean and between 90 cm and 110 cm total length Based on the above life history Caribbean Sea and has been reported (TL), with fully adult males observed at parameters, and following methods in along the coasts of Venezuela, Trinidad, sizes larger than 119 cm TL in the field Corte´s (2002) for estimating Guyana, Suriname, French Guiana, and (Lessa et al. 1999a). According to von survivorship, Casselberry and Carlson northern Brazil (Lessa et al. 2006a). The Bertalanffy growth parameters, size at Brazilian range includes the states of maturity is 103 cm TL for males and (2015a) estimated productivity (as Amapa´, Para´, and Maranha˜o, with about 115 cm TL for females (Lessa et intrinsic rate of population increase, ¥1 Tubara˜o Bay in Maranha˜o as its al. 2000), although the smallest ‘‘r’’) at 0.004 year (median) within a ¥ easternmost limit (Silva 2004; Lessa et pregnant female recorded was 118 cm range of 0.040–0.038 (5 percent and al. 1999a). The daggernose shark has long (Lessa et al. 1999a). After maturity 95 percent percentiles) (Carlson one of the smallest ranges of any is reached, growth rates decrease to less unpublished). Median generation time elasmobranch species (Lessa et al. than 10 cm/year (Lessa et al. 2000). was estimated at 10.6 years, the mean 2000). It is a coastal species that is Maximum age is estimated to be age of parents of offspring of a cohort commonly found in estuaries and river approximately 20 years based on (m1) was 10.7 years and the expected mouths in tropical climates and is most converting the length of a 160 cm TL number of replacements (R0) was 1.05. abundant in these areas during the female with parameters from the von Lessa et al. (2010) estimated annual Amazonian summer (i.e., the rainy Bertalanffy growth equation, although population growth to be r = ¥0.048 season) (Compagno 1984; Compagno the largest male caught was 144 cm TL, under natural mortality rates (of 0.28 1988; Lessa 1997; Lessa et al. 1999a; corresponding to an age of 13 years old, using the Hoenig (1984) method and Lessa et al. 2006b; Grace 2001). These and the oldest aged individuals from 0.378 using the Pauly (1980) method), sharks are often found in association vertebrae analyses were of a 7 year old and a generation time of 9 years. If with mangrove coastlines, occur in male and a 12 year old female (Lessa et fishing mortality rates were highly turbid waters and in low lying al. 2000). incorporated, the annual population and indented coastlines that can have The reproductive cycle of daggernose growth was estimated to be r = ¥0.074, tide changes that vary as much as 7 sharks in Brazil is synchronized with with a generation time of 8.4 years the rain cycle. The rainy season runs meters (m) (Martins-Juras et al. 1987; (Lessa et al. 2010). These demographic Lessa et al. 1999a). Daggernose sharks from January to June and the dry season parameters place daggernose sharks occur in water depths between 8 m and runs from July to December. A study by towards the slow growing end of the 40 m, temperatures ranging from 21.5 °C Lessa et al. (1999a) found that 70 to 31.5 °C and salinities between 13.96 percent of the pregnant females ‘‘fast-slow’’ continuum of population and 33.60 ppt (Lessa 1997; Lessa et al. collected during the study in the rainy parameters calculated for 38 species of 1999a, b). Salinity is considered a season were carrying a recently sharks by Corte´s (2002), which means determining factor for the distribution of fertilized egg or very small embryo, this species generally has a low the species, but does not prevent the suggesting that the ovulation period potential to recover from exploitation.

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Historical and Current Distribution and pressure, it is assumed that dramatic these sharks in gillnets ranging from Population Abundance population declines have occurred in 6.04 kilogram (kg)/km/hour up to 71 kg/ In Brazil, daggernose sharks were the last decade throughout this part of km/hour (during the peak in the rainy historically found in the states of the species’ range, similar to the levels season) in the early 1990s. However, Amapa´, Para´, and Maranha˜o, and were documented in Brazil, but scientific due to the species’ sensitive life history first formally recorded in surveys from data on population trends are severely traits, this high level of fishing mortality the 1960s in the state of Maranha˜o lacking for this region (Kyne et al. 2012). was found to be unsustainable, causing (Lessa 1986). In 1999, daggernose sharks Summary of Factors Affecting the the daggernose shark population to were documented as occurring in two Daggernose Shark decrease by 18.4 percent per year in the Marine Conservation Areas in northern 1990s. By 1999, the percentage of We reviewed the best available daggernose sharks in the artisanal Brazil, the Parque Nacional Cabo Orange information regarding historical, in Amapa´, and the Reentraˆncias gillnet bycatch along the Brazilian coast current, and potential threats to the had significantly decreased, with Maranhenses in Maranha˜o (Lessa et al. daggernose shark species. We find that 1999b). However, in recent years, the daggernose sharks comprising only the main threat to this species is around 7–10 percent of the absence of daggernose sharks in areas overutilization for commercial where they were previously common elasmobranch incidental catch (Lessa et purposes. We consider the severity of al. 1999b; Lessa et al. 2000). By 2004 has been noted. For example, in the this threat to be exacerbated by the Braganc¸a fish market in northern Brazil and 2006 the species was no longer species’ natural biological vulnerability observed or recorded in the states of (State of Para´), daggernose sharks were to overexploitation, which has led to once among the most common shark Para´ (Lessa et al. 2010) or Maranha˜o significant declines in abundance and (Almeida et al. 2011), respectively, species sold in the market. However, a subsequent extirpations from areas genetic analysis of shark carcasses based on data from research surveys where the species was once commonly conducted in these regions. collected from this fish market between found. We find current regulatory 2005 and 2006 found no evidence of measures inadequate to protect the Artisanal fisheries operating off Brazil daggernose sharks being sold in the species from further overutilization. continue to exert significant fishing market (Rodrigues-Filho et al. 2009). Hence, we identify these factors as pressure on the daggernose shark, which Although the species’ absence in fish additional threats contributing to the is likely contributing to fishing markets could indicate obeyance of species’ risk of extinction. We mortality rates that historically resulted Brazilian law, which prohibited the summarize information regarding these in the substantial decline of the species. catch of daggernose sharks in 2004, it threats and their interactions below As such, overutilization continues to be has been noted that these laws are according to the factors specified in a threat to the species as these fisheries poorly enforced and frequently ignored section 4(a)(1) of the ESA. Available are still highly active throughout its (see discussion of Inadequacy of information does not indicate that range. In fact, in the North region of Existing Regulatory Mechanisms below). habitat destruction or modification, Brazil (which includes the States of Additionally, while daggernose sharks disease, predation or other natural or Amapa´ and Para´), the artisanal sector were once caught abundantly in manmade factors are operative threats accounts for more than 80 percent of the Maranha˜o prior to 1992, they were on these species; therefore, we do not total landings from this region and notably absent in research surveys discuss these factors further in this represents around 40 percent of the total conducted from November 2006 to finding. See Casselbury and Carlson artisanal landings for the entire country. December 2007 (Almeida et al. 2011). (2015a) for discussion of these ESA These fisheries tend to be concentrated Based on the species’ life history section 4(a)(1) threat categories. in areas where the daggernose shark parameters and rates of fishing would most likely occur, including the mortality, population abundance was Overutilization for Commercial, Amazon River estuary, small estuaries estimated to have declined by 18.4 Recreational, Scientific, or Educational and bays, and shallow coastal waters percent per year for 10 years from the Purposes within the extensive mangrove area that mid-1990s to mid-2000, resulting in a Based on historical catch data and covers the northern coast of Brazil total population decline of over 90 trends, the primary threat to daggernose (Vasconcello et al. 2011). In the percent (Santana and Lessa 2002; Rosa sharks is overutilization in artisanal Northwest region of Brazil (which and Lima 2005; Kyne et al. 2012). fisheries. Given its rather shallow depth includes the States of Maranha˜o south Very little information is available on distribution, in Brazil, the species is to Bahia), the artisanal sector is also the the distribution and abundance of the bycaught in the artisanal gillnet dominant fishing sector, accounting for daggernose shark outside of Brazil. fisheries for Spanish mackerel more than 60 percent of the total While undated catch records exist (Scomberomorus brasiliensis) and king landings from this region. The king across the entire coastline of French weakfish (Cynoscion acoupa), which weakfish fishery, which was noted as Guiana, records are scarce throughout operate inside or near estuary mouths. one of the main artisanal gillnet Suriname, Guyana, and Trinidad and Historically, the species was caught in fisheries responsible for bycatching Tobago (Bigelow and Schroeder 1948; large numbers along the northern daggernose sharks, remains one of the Springer 1950; Compagno 1988; Global Brazilian coastline and represented a most important fisheries in Brazil as Biodiversity Information Facility (GBIF) significant component of the artisanal evidenced by the fact that the species 2013). Additionally, although Lessa et gillnet bycatch. For example, in the was the 4th most landed marine fish in al. (1999a) includes Venezuela as part of State of Para´, daggernose sharks terms of volume in 2011 (21,074.2 t; the daggernose shark range (citing represented close to 70 percent of the Ministe´rio da Pesca e Aquicultura Cervigo´n 1968), no other information artisanal catch in the 1980s during the (MPA) 2011). Together, the artisanal could be found regarding the present Amazonian summer (Lessa et al. 2010). landings from these regions represent existence of the daggernose shark in Farther south, off the Maranha˜o coast, over 80 percent of the total artisanal Venezuela. Given the species’ sensitive harvest of daggernose sharks would landings for the entire country biological traits to exploitation and begin in October and peak in January, (Ministe´rio do Meio Ambiente/Instituto evidence of high artisanal fishing with the catch per unit effort (CPUE) of Brasileiro do Meio Ambiente e dos

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Recursos Naturais Renova´veis (MMA/ being significantly underestimated (on however, the last time they were IBAMA) 2007). the order of 2.6 times for Trinidad and reported in these areas was in 1999. These artisanal fishing practices and Tobago (Mohammed and Lindop 2015); Although Brazil has a number of effort levels, which caused declines in 1.6 times for Guyana (Macdonald et al. regulations in place to protect daggernose shark populations off Brazil, 2015); 3.4 times for Suriname (Hornby endangered or threatened species, like are likely similar in Venezuela, Trinidad et al. 2015); and 4 times for French the ones described above for daggernose and Tobago, Guyana, Suriname, and Guiana (Harper et al. 2015)), daggernose sharks, it is generally recognized that French Guiana (which comprises the sharks are not specifically identified in these regulations are poorly enforced, other half of the species’ range). These the catches (Shing 1999). However, particularly within artisanal fisheries countries have a substantial artisanal historical and more recent information (Lessa et al. 1999b; Amaral and fishing sector presence, with catches suggests daggernose sharks were and Jablonski 2005; Almeida et al. 2011; from artisanal fishing comprising up to may still be utilized. Although the value Rodrigues-Filho et al. 2012). Poverty, 80 percent of the total fish landings. In of daggernose shark fins is low, its meat lack of education within the artisanal French Guiana, sharks alone comprised has been sold in markets from artisanal fisheries sector, and increased artisanal 40.4 percent of the annual artisanal fisheries for decades (Lessa et al. 2006a), fishing effort, especially in the State of landings for the local market (Harper et with Bigelow and Schroeder (1948) Maranha˜o, have already contributed to al. 2015). However, as noted in the recording daggernose shark meat in the decline of many elasmobranch Inadequacy of existing regulatory markets in Trinidad and Tobago and populations, including the daggernose mechanisms section, due to minimal noting its likelihood in markets in shark (Lessa et al. 1999b), despite the controls of these artisanal fisheries, Guyana. Therefore, given the evidence existence of protective legislation and including lack of enforcement of utilization of the species, as well as marine protected areas. As such, capabilities of existing regulations, the the significant fishing effort by artisanal effective conservation appears to be available data indicate that many of fishing fleets throughout the daggernose lacking in Brazil (Lessa et al. 1999b; these country’s coastal marine resources shark range, including unregulated Amaral and Jablonski 2005), with are fully to overexploited (Food and access to fishing grounds where the existing regulatory mechanisms likely Agriculture Organization of the United shark occurs, the observed absence of inadequate to protect the daggernose Nations (FAO) 2005a, 2005b, 2006, the daggernose shark in recent years can shark from further fishery-related 2008). In Trinidad and Tobago, for likely be attributed to overutilization of mortality. example, it is estimated that the the species to the point where In December 2014, the Brazilian artisanal fleet catches between 75 and overutilization is significantly Government’s Chico Mendes Institute 80 percent of the total landings from contributing to its risk of extinction. for Biodiversity Conservation approved these islands (FAO 2006). Of concern, as an FAO National Plan of Action (NPOA) it relates to overutilization of the Inadequacy of Existing Regulatory for the conservation of sharks (hereafter daggernose shark, is the fact that Mechanisms referred to as FAO NPOA-sharks) for Trinidad and Tobago have an open Throughout the species’ range, Brazil (No. 125). The plan considers the access fishery for the artisanal sector, species-specific protection for daggernose shark to be one of the which means there are no restrictions daggernose sharks is only found in country’s 12 species of concern and on the numbers and types of vessels, Brazil. In 2004, the daggernose shark recommends a moratorium on fishing fishing gear, or trips (FAO 2006; was first listed in Annex I of Brazil’s with the prohibition of sales until there Mohammed and Lindop 2015). In other endangered species list: ‘‘Lista Nacional is scientific evidence in support of words, any local vessel is allowed to Oficial de Espe´cies da Fauna recovery (Lessa et al. 2005). enter the fishery and catch as much they Ameac¸adas de Extinc¸a˜o—Peixes e Additionally, it proposes the expansion can handle, with no restriction on Invertebrados Aqua´ticos’’ (Silva 2004). of the Reentraˆncias Maranhenses (where fishing effort (FAO 2006). Similarly, An Annex I listing prohibits the catch daggernose sharks were observed in Guyana also operates an open access of the species except for scientific 1999) to include the marine coastal zone fishery for its artisanal gillnet sector. purposes, which requires a special and banks, providing additional Given that artisanal fishing for license from the Brazilian Institute of protection to the sharks from potential groundfish in Guyana, which comprises Environment and Renewable Resources fishery-related mortality. The plan one of the country’s two main fishing (IBAMA) (Silva 2004). This protection recommends increased effort monitoring activities (the other being direct was renewed in December 2014, when of vessels using nets in the area and exploitation of shrimp by trawlers), is the daggernose shark was listed as increased education to encourage the predominantly conducted using gillnets, ‘‘critically endangered’’ on the most release of live daggernose sharks and open access fisheries cover a significant recent version of the Brazilian prevent the landing of the species. In portion of the fishery sector for the endangered species list approved by the general the plan sets short term goals for country (FAO 2005a). Ministry of the Environment (Directive improved data collection on landings As noted above, this essentially No 445). ‘‘Critically endangered’’ on this and discards, improved compliance and unregulated artisanal fishing throughout list is defined as a species that presents monitoring by the IBAMA, supervision the Atlantic Caribbean, employing an extremely high risk of extinction in of elasmobranch landings to ensure fins unselective net gear and concentrated in the wild in the near future due to are landed with carcasses, the creation inshore coastal waters where daggernose profound environmental changes or of a national port sampler program, and sharks would primarily occur, has led to high reduction in population, or intensified on-board observer the overexploitation of many marine significant decrease in the taxon’s range. monitoring programs. Mid-term goals species, including sharks. However, In addition to the landing prohibition, include increased monitoring and there is virtually no information daggernose sharks also receive enforcement within protected areas as available on daggernose shark catches protection when they occur within two well as the creation of new protected from the Caribbean countries in the of Brazil’s marine protected areas areas based on essential fish habitat for daggernose shark range. These countries (MPAs): The Parque Nacional Cabo the 12 species of concern. It also calls report general shark landings to the Orange and the Reentraˆncias for improved monitoring of fishing from FAO but, in addition to these catches Maranhenses (Lessa et al. 1999b); beaches in coastal and estuarine

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environments. Long term goals call for Extinction Risk within a range of ¥0.040–0.038 improved ecological data and stock Although accurate and precise (Carlson unpublished). Under natural assessments for key species as well as population abundance and trend data mortality rates, Lessa et al. (2010) mapping of elasmobranch for the daggernose shark are lacking, estimated annual population growth to ¥ spatiotemporal distributions. This data best available information provides be negative, with an r = 0.048 and a will be used to better inform the multiple lines of evidence indicating generation time of 9 years. When fishing creation of protected areas and seasonal that this species currently faces a high mortality was considered, the estimate ¥ fishing closures. However, as stated risk of extinction. Below, we present the of r decreased even further, to 0.074, above, the plan was only just approved demographic risk analysis, threats with a generation time of 8.4 years. as of December 2014, and will not be assessment, and overall risk of Considering the daggernose shark has fully implemented for another 5 years. extinction for the daggernose shark. already undergone substantial population declines, and is still Even if the recommendations outlined Demographic Risk Analysis in the plan are implemented in the susceptible to fishing mortality in the future, it remains uncertain if they will Abundance active artisanal fisheries throughout its range, the species’ extremely low be effective as the best available There is a significant lack of productivity (with estimates of negative information suggests that current abundance information for I. annual population growth rates) is regulatory measures in Brazil to protect oxyrhynchus throughout its range. In likely significantly contributing to its vulnerable species are poorly enforced, northern Brazil, the relatively recent risk of extinction. particularly within artisanal fisheries. (2004–2009) absence of the species in Outside of Brazil, there is limited fish markets where they were once Spatial Structure/Connectivity abundantly sold, in addition to their information on shark fishing regulations absence in fishery-independent research Very limited information is available or their adequacy for protecting surveys in areas where they were regarding spatial structure and daggernose sharks from overutilization. commonly caught prior to 1992, connectivity of the daggernose shark In Guyana and Trinidad and Tobago, suggests the species has suffered populations. The best available gillnet fisheries are restricted to using significant declines in population information suggests the daggernose nets of 900 ft or less with no more than abundance. Based on the daggernose shark has a very restricted range, one of a 15-foot depth; however, currently, shark’s life history parameters and rates the smallest of any elasmobranch there are no minimum size restrictions of fishing mortality, the population species, and, as such, an increased or catch quotas for sharks in either abundance in northern Brazil is vulnerability to extinction from country (Shing 1999). As mentioned estimated to have declined by 18.4 environmental or anthropogenic previously, both countries have open percent per year from the mid-1990s to perturbations. In addition, the access fisheries (however, in Guyana the mid-2000, resulting in a total population substantial declines in the Brazilian open access fishery only applies to the decline of at least 90 percent in population and subsequent absence of artisanal gillnet fishery) (FAO 2005a, approximately half of the species’ the species in areas it was previously 2006). In the late 1990s a fisheries known range. Although abundance known to occur, as well as its rarity management plan was drafted for information from the other parts of the throughout the rest of its range, suggest Trinidad and Tobago, which prohibited species’ range, including off Venezuela, the species likely exists as patchy and the use of monofilament gillnets less Trinidad, Guyana, Suriname and French small populations, which may limit than 4.75″ stretch mesh and developed Guiana, is presently unavailable, it is connectivity. However, there is not a licensing system (Shing 1999); thought that these populations have enough information to identify critically however, no further details about the suffered similar declines based on the important populations to the taxon as a plan, including effectiveness or species’ biological vulnerability and whole, or determine whether the rates of enforcement of these regulations, could susceptibility to artisanal fisheries dispersal among populations, metapopulations, or habitat patches are be found. According to Casselberry and operating in these areas. Given the presently posing a risk of extinction. Carlson (2015a), in the summer of 2013, continued artisanal fishing pressure Guyana’s Fisheries Department within throughout the species’ range, coupled Diversity the Ministry of Agriculture passed a 5- with the species’ present rarity and its The loss of diversity can increase a year Fisheries Management Plan for potential extirpation in areas where it species’ extinction risk through Guyana to run from 2013 to 2018, with was previously abundant, it is likely decreasing a species’ capability of one aspect of this plan meant to address that the species is still in decline, with current abundance trends and levels responding to episodic or changing shark fishing, but no further details environmental conditions. This can could be found at this time. contributing significantly to its risk of extinction. occur through a significant change or Enforcement of existing fishery loss of variation in life history regulations is also lacking due to Growth Rate/Productivity characteristics (such as reproductive insufficient resources, with minimal The daggernose shark has extremely fitness and fecundity), morphology, control over the fisheries resulting in low productivity. Litter sizes range from behavior, or other genetic increasing competition and conflicts 2–8 pups, with a 1-year gestation period characteristics. Although it is unknown among fishermen and between fishing and a year of resting between if I. oxyrhynchus has experienced a loss fleets and, consequently, overfishing of pregnancies. In other words, annual of diversity, the significant decline marine resources (FAO 2005a, 2005b, fecundity averages only 1–4 pups estimated for the population in northern 2006, 2008). No other pertinent because of the species’ biennial Brazil (comprising approximately half of information could be found on shark reproductive periodicity. Using these its known range), as well as the likely fishing regulations or their adequacy in life history parameters, Casselberry and small populations elsewhere throughout controlling the exploitation of sharks, Carlson (2015a) estimated a productivity its range, suggest the species may be at and more specifically daggernose (as the intrinsic rate of population an increased risk of random genetic drift sharks. increase) of r = 0.004 year¥1 (median) and could experience the fixing of

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recessive detrimental genes, reducing In 2004, the daggernose shark was extinction risk for the species. We seek the overall fitness of the species. listed on Brazil’s endangered species additional information on other list, and as of 2014, was classified as conservation efforts in our public Threats Assessment ‘‘critically endangered.’’ Additionally, it comment process (see below). The primary threat to the daggernose is listed as one of 12 species of concern Proposed Determination shark is overutilization in artisanal under Brazil’s FAO NPOA-sharks. fisheries. In Brazil, the species is However, the implementation and Based on the best available scientific bycaught in the artisanal gillnet effectiveness of the recommendations and commercial information as fisheries for Spanish mackerel and king outlined in this plan remain uncertain, presented in the status review report weakfish. Historically, the species with the best available information and this finding, we find that the comprised up to around 70 percent of indicating that current regulatory daggernose shark is presently in danger the artisanal catch during the measures in Brazil to protect vulnerable of extinction throughout its range. We Amazonian summer in the State of Para´, species are poorly enforced, particularly assessed the ESA section 4(a)(1) factors and was caught in large numbers by the in artisanal fisheries (the fishery sector and conclude that that the species faces artisanal gillnet fisheries operating on that poses the biggest threat of ongoing threats from overutilization and the Maranha˜o coast in Brazil. However, overutilization of the species). In inadequacy of existing regulatory given the extremely low productivity of addition, there appears to be a lack of mechanisms throughout its range. The the species and vulnerability to adequate fishing regulations to control species’ natural biological vulnerability depletion, this level of exploitation the exploitation of the daggernose shark to overexploitation and present resulted in substantial declines in the other parts of its range, and, as demographic risks (e.g., low and (estimated at over 90 percent) to the such, the inadequacy of existing declining abundance, negative point where the species is no longer regulatory measures is a threat that population growth rates, small, found in fish markets or observed in further contributes to the extinction risk fragmented and likely isolated trawl and research survey data. The of the species. populations, extremely restricted artisanal gillnet fisheries that were distribution, and very low productivity) responsible for this decline are still Risk of Extinction are currently exacerbating the negative active throughout the species’ range and Although there is significant effects of the aforementioned threats, likely exerting similar fishing pressure uncertainty regarding the current placing this species in danger of that historically resulted in the abundance of the species, the species’ extinction. We also found no evidence substantial decline of the daggernose population growth rate and productivity of protective efforts for the conservation shark populations. In fact, together, the estimates indicate that the species has of daggernose shark that would reduce artisanal landings from the North region likely suffered significant population the level of extinction risk faced by the of Brazil (which includes the States of declines (of up to 90 percent) species. We therefore propose to list the Amapa´ and Para´) and Northwest region throughout its range and will continue daggernose shark as an endangered (which includes the States of Maranha˜o to decrease without adequate protection species. south to Bahia), the areas where from overutilization. The species’ Brazilian Guitarfish (Rhinobatos daggernose sharks were once restricted coastal range, combined with horkelii) historically abundant, represent over 80 its recent (2004–2009) absence in areas percent of the total artisanal landings for where it was once commonly found, as Species Description the entire country, indicating the well as its present rarity throughout the The Brazilian guitarfish (Rhinobatos importance and, hence, likely rest of its range (with the last record of horkelii) is a member of the order continuation of this type of fishing in the species from 1999) indicate Rajiformes and the family Rhinobatidae these regions. Notably, the king potential local extirpations and suggest (Lessa and Vooren 2007). The species weakfish fishery, which was reported as an increased likelihood that the species within the family Rhinobatidae are very one of the two main artisanal gillnet is strongly influenced by stochastic or similar morphologically, which can fisheries responsible for bycatching depensatory processes. This make them difficult to distinguish from daggernose sharks, remains one of the vulnerability is further exacerbated by each other (De-Franco et al. 2010). The most important fisheries in Brazil. the present threats of overutilization Brazilian guitarfish has long nostrils Artisanal gillnet fisheries are also and inadequacy of existing regulatory with transversely flat or a slightly active in the other parts of the species’ measures that will significantly convex crown and has a median row of range, including Venezuela, Trinidad contribute to the decline of the existing tubercles (nodules) on its dorsal surface and Tobago, Guyana, Suriname, and populations (based on its demographic that are large and thorn-like (Lessa and French Guiana, with likely similar risks) into the future, compromising the Vooren 2005). The disc width is about fishing practices. Although landings species’ long-term viability. Therefore, 5/6 of the body length, with dorsal fins data from these countries are unknown, based on the best available information that are triangular and similar in size the available information suggests that and the above analysis, we conclude (Bigelow and Schroeder 1953). The artisanal fishing pressure is high and that I. oxyrhynchus is presently at a high dorsal side of the Brazilian guitarfish is that the species has been taken in small risk of extinction throughout its range. olive grey or chocolate brown in color numbers by local fishermen in these Protective Efforts and lacks light or dark markings. countries, with daggernose sharks Additionally, its snout has a ‘‘sooty’’ historically sold in markets in Trinidad With the exception of the oval patch (Lessa and Vooren 2005). and likely Guyana. Given the species’ recommendations within Brazil’s FAO susceptibility to depletion from even NPOA-sharks (discussed above), we Range and Habitat Use low levels of fishing mortality, it is were unable to find any other The Brazilian guitarfish is found highly likely that overutilization by information on protective efforts for the along the coast of South America in the artisanal fisheries operating throughout conservation of daggernose sharks in southwestern Atlantic from Bahia, the species’ range is a threat that is Brazil, Venezuela, Trinidad and Tobago, Brazil to Mar del Plata, Argentina significantly contributing to its risk of Guyana, Suriname, or French Guiana (Figueiredo 1977; Lessa and Vooren extinction. that would potentially alter the 2005, 2007; GBIF 2013). Newborns and

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juveniles live year round in coastal and summer to give birth. Litter sizes et al. 2005b), but no follow-up surveys waters less than 20 m deep. Adults range from 4–12 pups and increase with were conducted after 2005. coexist with immature individuals in female size (Lessa and Vooren 2005). Throughout the rest of its range, there shallow waters between November and Genetics and Population Structure is little information on the abundance of March, when pupping and mating R. horkelli, with the species considered occur, but spend the rest of the year Studies examining the genetics of the to be a rare occurrance. In northern offshore in waters greater than 40 m species or information on its population Argentina (34° S.–43° S.), estimated depth. In the winter, individuals can be structure could not be found. found in water temperatures as low as mean biomass of Brazilian guitarfish 2 9 °C, while in the summer, individuals Demography was 0.1240 t/nm between 1981 and 1999, with R. horkelli comprising only are found in average water temperatures Total natural mortality for Brazilian ° 0.44 percent of the biomass of demersal of 26 C (Lessa and Vooren 2005). guitarfish was estimated by Caltabellota Brazilian guitarfish are commonly found (2014) using an age at maturity of 5 fish on the northern Argentine in salinities ranging from 24–28 ppt in years (i.e., an earlier age of maturity continental shelf (Jaureguizar et al. northern Argentina (Jaureguizar et al. than what was reported by Vooren et al. 2006). In 1981, biomass of Brazilian 2006). (2005a)), and found the estimated total guitarfish was calculated to be 0.010 t/ 2 Diet and Feeding natural mortality from catch curves to nm in 1981. Estimated biomass then be 0.692 for males and 0.751 for peaked at 0.441 t/nm2 in 1994 before There is very little information on the 2 females. Modeling of various falling steadily to 0.007 t/nm in 1999 diet or feeding behavior of Brazilian exploitation scenarios found that under (Jaureguizar et al. 2006). Biomass guitarfish. Refi (1973) recorded the natural conditions, with no fishing estimates reported in Argentina’s FAO stomach contents of six individuals mortality, the population would NPOA-sharks for the coast of Buenos caught in Mar del Plata, Argentina and increase by 9 percent each year, with a Aires province and Uruguay were 2,597 found that stomachs contained the population doubling time of 7.41 years Patagonian octopus (Octopus t in 1994, 661 t in 1998, and 91 t in 1999 tehuelchus), shrimp (Hymenopeneus (Caltabellota 2014). In the presence of (Argentina FAO NPOA-sharks 2009). muelleri), decapods, isopods, and fishing mortality and an age at first Along the oceanic coast of Uruguay, R. polychaetes. No other information on capture of 2 years, the Brazilian horkelii occurs with low density, with diet or feeding could be found. guitarfish population would decline by annual catches around 3 t in 2000 and 25 percent every 2.73 years; however, if 2001 (Meneses 1999; Paesch and Growth and Reproduction the age at first capture was after the age Sunday 2003). Based on a yearly vertebral annulus at first maturity (assumed to be 5 years formation in September, Vooren et al. for these models), the population would Summary of Factors Affecting the (2005a; citing Lessa (1982)) report the increase by 4 percent each year Brazilian Guitarfish (Rhinobatos von Bertalanffy growth rate (k) for (Catabellota 2014). Based on the life horkelii) Brazilian guitarfish to be 0.0194, with a history parameters discussed We reviewed the best available theoretical maximum size of 135.5 cm previously, these demographic information regarding historical, TL and age at maturity between 7 and parameters indicate that the Brazilian 9 years for females and 5 and 6 years for guitarfish generally has a low potential current, and potential threats to the males. Similar results were estimated by to recover from exploitation, Brazilian guitarfish species. We find Caltabellota (2014), with a theoretical particularly if the species is that the main threat to this species is maximum size of 121.71 cm TL and k experiencing fishing pressure on overutilization for commercial = 0.21. No significant differences were neonates and juveniles. purposes. We consider the severity of this threat to be exacerbated by the found in growth between the sexes. Historical and Current Distribution and species’ natural biological vulnerability Using two different methods, Population Abundance Caltabellota (2014) also estimated to overexploitation, which has led to theoretical longevity of 18.24 and 14.17 The Brazilian guitarfish is distributed significant declines in abundance of all years for females, and 13.86 and 10.90 along the coast of South America, from life stages, particularly neonates. We years for males. Vooren et al. (2005a) Bahia, Brazil to Mar del Plata, find current regulatory measures found longevity to be longer for both Argentina. The species’ center of inadequate to protect the species from females and males, with estimates of 28 distribution lies between 28° and 34° S. further overutilization. Hence, we years and 15 years, respectively. and also corresponds to the area where identify these factors as additional Size at maturity for Brazilian it is most abundant. This area is known threats contributing to the species’ risk guitarfish is between 90 cm and 120 cm as the Plataforma Sul, which includes of extinction. We summarize TL for both sexes; the smallest pregnant the continental shelf of southern Brazil information regarding these threats and females recorded were between 91–92 and extends from Cabo de Santa Marta their interactions below according to the cm TL, and all captured females larger Grande (28°36′ S.) to Arroio Chuı´ ° ′ factors specified in section 4(a)(1) of the than 119 cm TL were pregnant (Lessa et (33 45 S.). In historical bottom trawl ESA. Available information does not al. 2005a; Lessa and Vooren 2005). The surveys between latitudes 28°00′ S. and indicate that habitat destruction or Brazilian guitarfish has an annual 34°30′ S., R. horkelii was common curtailment, disease, predation or other reproductive cycle, with lecithotrophic across the Plataforma Sul south of development (i.e., larva depend on the latitude 29°40′ S. (Vooren et al. 2005a). natural or manmade factors are egg’s yolk reserve supplied by the Annual catch of Brazilian guitarfish in operative threats on these species; mother), and a gestation period lasting this area was approximately 636 t–1803 therefore, we do not discuss these approximately 11–12 months (Lessa et t from 1975–1987 (Miranda and Vooren factors further in this finding. See al. 2005a; Lessa and Vooren 2005). 2003). Research surveys conducted Casselbury and Carlson (2015b) for Gravid females live at depths greater between Chuı´ and Solida˜o (Rio Grande discussion of these ESA section 4(a)(1) than 20 m for most of the year, but do Sul, Brazil) in February 2005 found threat categories. migrate into the shallows in the spring an average CPUE of 1.68 kg/hr (Vooren

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

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artisanal fishermen, the species is not significantly declined, causing the stock fishery-related mortality over their usually released, despite its prohibited to collapse after 1986. entire habitat. status (Vooren et al. 2005a; Vieira 2014). Overutilization still remains a threat Inadequacy of Existing Regulatory For example, from November 2013 to to the species as fishing by the Mechanisms March 2014, Vieira (2014) monitored industrial and artisanal fleets continues Like the daggernose shark, the four artisanal fishing boat operations to occur at high efforts on the (off Rio Grande do Sul) that made 50 Brazilian guitarfish was also listed on Plataforma Sul and especially within sets over 20 fishing trips in depths of 5 Brazil’s endangered species list in 2004, important nursery habitats for the m to 21 m using primarily gillnets. The and as of 2014, was classified as species (Vooren et al. 2005a; Klippel et Brazilian guitarfish was the second most ‘‘critically endangered.’’ In 2007, Lessa abundant species caught by gillnets, al. 2005; Vooren and Klippel 2005c). In and Vooren noted that the 2004 with 125 individuals captured, 2007, the industrial fleets operating off prohibition on catching the species was representing 17.5 percent of southern Brazil, where R. horkelli is gradually becoming more effectively elasmobranch catch. Its frequency of most concentrated, and specifically enforced, but genetic studies indicate occurrence per fishing trip was 40 from the States of Parana, Santa that enforcement was still relatively percent. The author noted that all of the Catarina, and Rio Grande du Sol poor as recently as 2009. Of 267 caught sharks (either as catch or (identified as Brazil’s ‘‘South Region’’), guitarfish samples that were collected at bycatch) were sold, whereas out of all were responsible for landing around 54 ports throughout southeastern and the caught rays, only R. horkelli was percent (151,154 mt) of the total southern Brazil between 2008 and 2009, sold. Additionally, although the CPUE industrial fish catch for all of Brazil 55.8 percent were genetically identified was estimated to be relatively low for (277,364.5 mt). Within Brazil’s South as Brazilian guitarfish (De-Franco et al. the elasmobranchs in the study, given Region, the industrial fleet comprised 2012). Of the 85 samples from boats the area where these artisanal fisheries 59.3 percent of the total fish landings operating off Santa Catarina, 100 operate, the majority of the R. hokelli from the region (255,080.5 mt). In 2011, percent of the guitarfish were Brazilian catch consisted of immature individuals the South Region’s marine fish landings guitarfish (De-Franco et al. 2012). When and breeding adults (with observations (not including aquaculture) amounted to the fishermen were asked about their of pregnant females initiating abortion 158,515.4 mt, representing 47 percent of landings during sample collection, on the boats) which likely compromises the total fish production from that many of them denied harvest of recruitment to the already at risk region and 28.6 percent of the national guitarfish, suggesting that fishermen are population (Vieira 2014). total of marine fish landings. In terms of aware of the capture prohibition of The substantial abundance declines of artisanal fisheries, fishing pressure (and Brazilian guitarfish (De-Franco et al. R. horkelli on the Plataforma Sul due to related mortality) on R. horkelli is likely 2012). However, because fishermen overutilization by fisheries, as indicated high given that the mullet fishery, the commonly remove the head and gut of by the commercial and artisanal target of artisanal fisheries operating any guitarfish before arriving in port, fisheries data, is further confirmed by within R. horkelli nursery habitats, is an distinguishing the Brazilian guitarfish CPUE data from fishery-independent important fishery in Brazil. According from the other two guitarfish species in surveys of the region. On the Plataforma to Lemos et al. (2014), catches of mullets the area (R. percellens and Zapteryx Sul, a number of research cruises dating (Mugil liza) in Rio Grande do Sul and brevirostris) is difficult, which, when coupled with the lack of adequate back to 1972 have surveyed the area Santa Catarina between 1997 and 2010 government inspections, may be using bottom trawl gear (from depths of were around 95 percent of the total encouraging fishermen to disregard the around 10 m to over 500 m). In an catch from all other Brazilian states, law for economic gain (De-Franco et al. analysis of this time series set, Vooren Uruguay, and Argentina. In 2011, et al. (2005a) note that between the 2012). Similarly, and most recently, a mullets were the 2nd most landed fish 2013 investigation by Sea Shepherd periods of 1975–1986 and 1993–1999, (in terms of volume) in the artisanal CPUE of R. horkelli showed similar Brazil into the illegal trade of fisheries in Rio Grande do Sul (IBAMA/ declines as those observed in the elasmobranchs by the Sa˜o Paulo General Centro de Pesquisa e Gesta˜o dos commercial CPUE over the same period. Warehousing and Centers Company led Recursos Pesqueiros Lagunares e Based on the CPUE trends, abundance to the seizure of 700 kg of illegal Estuarinos (CEPERG) 2012) and the 5th of R. horkelli on the Plataforma Sul in elasmobranch species by federal police. depths of 20 m–200 m is estimated to most landed marine fish species for all Included in the illegal haul were have decreased by about 85 percent of Brazil, with landings totaling 18,045 Brazilian guitarfish, again suggesting between 1975 and 1999 (Vooren et al. t (MPA 2011), suggesting that this that poor enforcement of present 2005a). significant fishing effort by artisanal regulations is likely contributing to the Overall, based on the above fisheries in the inshore pupping continued exploitation and, commercial and artisanal fishing data, it grounds of Brazilian guitarfish is consequently, overutilization of the is estimated that over the period of unlikely to decrease in the foreseeable species. 1975–1986, around 100,000 mature R. future. Additionally, the relatively Although the Brazilian guitarfish horkelli females and 100,000 mature R. recent expansion and operation of the occurs in several MPAs within Brazilian horkelli males were caught annually Rio Grande do Sul and Itajai trawl fleets waters, including APA de Canane´ia- (Vooren et al. 2005a). The removal of on the outer shelf and continued Iguape-Peruı´be (Sa˜o Paulo; 234,000 these reproductively active adults from operation of the pair trawl fleet on the hectares), PARNA do Superagui (Parana; the population translated to a loss of inner continental shelf suggest 33,988 hectares), REBIO do Arvoredo around 600,000 newborns per year, or overutilization (in the form of bycatch (Santa Catarina; 17,600 hectares) and 6.7 million newborns over the course of mortality) is still a threat to the species. RESEX Marinha do Pirjubae´ (Santa the 11-year period of fishing, and led to Areas that previously served as offshore Catarina; 1,712 hectares) (Rosa and Lima recruitment overfishing of the species refugia for the Plataforma Sul 2005), these MPAs only protect the (Vooren et al. 2005a). As a result of this population from fishing pressure are no species from exploitation when they overutilization, abundance of the longer protected from exploitation, with occur within these areas. In addition, species on the Plataforma Sul both juveniles and adults susceptible to the coverage of these MPAs compared to

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the range of the species is very small longer grant new licenses that would based on the best available information and also located north of the center of allow for such fishing; forbid processing (including fisheries-independent survey distribution and concentration of the and marketing of the species; and data), it appears that the species has species and, therefore, unlikely to promote safe release if possible. likely undergone significant declines significantly decrease the threat of However, updated results from the goals throughout its range. Given the overutilization to the species. and priorities of this plan could not be continued high fishing pressure in the Another regulation in place in Brazil found. As such, their implementation species’ nursery grounds and presence to control the exploitation of marine and overall effectiveness at decreasing of the species in recent landings data resources is a prohibition on trawl the threats to the species remains highly despite its prohibited status, abundance fishing within three nautical miles (nm) uncertain. has likely continued to decline. from the coast of southern Brazil. This prohibition may help decrease fishery- Extinction Risk Growth Rate/Productivity related mortality of R. horkelli in the The best available information Lessa and Vooren (2005) estimated nearshore areas primarily used as provides multiple lines of evidence the growth rate of R. horkelii as (k) = nursery habitat by the species; however, indicating that the R. horkelli currently 0.194, and more recently, Caltabellota according to Chiaramonte and Vooren faces a high risk of extinction. Below, (2014) reported similar results, with an (2007), enforcement of this prohibition we present the demographic risk estimated k = 0.21 (with no significant has been noted as difficult. In addition, analysis, threats assessment, and overall difference in growth rates between the species is still susceptible to being risk of extinction for the Brazilian sexes). The species is thought to caught as bycatch in the legally guitarfish. reproduce annually, with a long permitted coastal gillnet fisheries gestation period (∼1 year) and low (which also operate in nursery areas) Demographic Risk Analysis fecundity (litter sizes range from 4 to 12 and in the offshore trawl and gillnet Abundance pups). Females have also been observed fisheries and vulnerable to the aborting embryos upon capture in There is very limited information associated bycatch mortality (Lessa and fishing gear, further decreasing the regarding abundance estimates for R. Vooren 2007). Therefore, the adequacy reproductive output of the species. In horkelli throughout its range. The of the trawl prohibition in decreasing addition, based on the data, it appears majority of the Brazilian guitarfish fishery-related mortality of R. horkelli to that both males and females of the population and center of distribution is the point where the extinction risk of ° ° species do not reach reproductive the species is significantly lowered is concentrated between 28 S. and 34 S. maturity until they have grown to unclear. in southern Brazil, and it is scarce approximately 74–89 percent of their elsewhere. On the northern Argentine maximum size. These reproductive Like the daggernose shark, the ° continental shelf, between 34 S. and characteristics suggest the species has Brazilian guitarfish is one of Brazil’s 12 ° species of concern identified in their 43 S., which appears to be the southern relatively low productivity, similar to FAO NPOA-sharks. The plan extent of the species’ range, mean other elasmobranch species, which recommends a moratorium on fishing biomass of R. horkelli has fluctuated likely hinders its ability to quickly with a prohibition of sales until there is over the years. In 1981, biomass was rebound from threats that decrease its scientific evidence in support of estimated to be 0.010 t/nm2. Biomass abundance (such as overutilization). recovery, and proposes a fishing peaked in 1994 at 0.441 t/nm2 before Under natural mortality, Caltabellota exclusion area over a large region of the falling to 0.007 t/nm2 in 1999 (2014) estimated that the population coast of Rio Grande do Sul at depths of (Jaureguizar et al. 2006). This represents would increase by 9 percent each year, 20 m to protect nursery areas (No 125, a 98 percent decrease from peak doubling every 7.41 years. However, if Lessa et al. 2005). As noted in the biomass between 1994–1999, but only a individuals of the species are fished daggernose shark analysis above, this decrease of around 30 percent from before reaching maturity (assumed to be plan will not be fully implemented for estimates in 1981. While mean 5 years), the Brazilian guitarfish another 5 years and it remains uncertain abundance estimates from the presumed population will decline by 25 percent whether the recommendations will be center of the species’ distribution are every 2.73 years (Caltabellota 2014). implemented and effective, as the best not available, we can infer significant Given the historical declines in CPUE available information suggests that historical population declines from a and levels of neonate and juvenile current regulatory measures in Brazil to variety of fishery effort, catch and landings, the species was likely subject protect the Brazilian guitarfish are landings data from this region. Based on to this exploitation scenario and poorly enforced. both fishery-independent sampling and subsequently experienced a negative Similar to Brazil, Uruguay also lists commercial fleet CPUE data from 1975– population growth rate to the point the Brazilian guitarfish as a species of 1986 and 1993–2002, the population of where the population collapsed after high priority in its FAO NPOA-sharks Brazilian guitarfish along the southern 1986. With the continued fishing (Domingo et al. 2008). The plan sets coast of Brazil has significantly pressure by the mullet fisheries short-term goals (12–18 months) to decreased in size. Data from the single operating in the nursery habitats and the investigate distribution and habitat use and pair trawl fleets operating on the industrial fisheries on the Plataforma and generate time-series of effort and Plataforma Sul indicate that CPUE Sul, the available data on growth rate catch; mid-term goals (24–30 months) to declined by 61 percent and 74 percent, and productivity of the species indicates conduct an abundance assessment and respectively, between the periods of that current exploitation levels will determine maximum sustainable catch 1975–1986 and 1993–2002 (Klippel et likely continue to cause population limits; and long term goals (36–48 al. 2005). The population is assumed to declines in the species, with no months) to conduct age, growth, have collapsed after 1986. Since 1993, information to suggest this trend is reproduction, and diet studies. In its the population is estimated to be about reversing. plan, Uruguay made it a priority to: 16 percent of its 1986 level. Due to Review current fishing licenses that species identification issues, there is Spatial Structure/Connectivity allow for the catch of Brazilian some level of uncertainty regarding the The species is thought to have a guitarfish and possibly modify them; no accuracy of the available data; however, continuous distribution along the

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Plataforma Sul (where the species is m depth), the shallow nursery areas, population from fishing pressure are no most abundant) (Vooren et al. 2005a); where neonates are found year-round longer protected from exploitation. however, there is no information on the and where adults are concentrated In July 2010, the State of Sa˜o Paulo, connectivity among other R. horkelii during the pupping and mating season, Brazil, declared the stock of Brazilian populations throughout the rest of its are still accessible to and heavily fished guitarfish collapsed due to intense range, including the importance of the by artisanal fisheries using gillnets and exploitation. Despite the species’ listing Plataforma Sul population to the taxon beach seines. For example, in the mullet under Brazil’s endangered species list as a whole. Based on the available data, fishery, fishermen use beach seines to since 2004, which effectively prohibits there is not enough information to trap the mullets; however, due to the catching this species, R. horkelli identify critical populations or low selectivity of the fishing gear, these continues to be brought into ports determine whether the rates of dispersal seines may also catch large numbers of throughout southeastern and southern among populations, metapopulations, or juvenile and pregnant female guitarfish Brazil. In both Brazil and Uruguay, R. habitat patches are posing a risk of as evidenced by the historical data from horkelli is considered a species of high extinction to the species. beach seine operations on the coast of priority under the country’s respective FAO NPOA-sharks. However, the Diversity Rio Grande do Sul (Miranda and Vooren 2003; Lessa and Vooren 2005; Vooren et implementation and effectiveness of the The loss of diversity can increase a al. 2005a). The mullet fishery remains recommendations outlined in these species’ extinction risk through an important fishery in Brazil and in plans remain uncertain, with the best decreasing a species’ capability of 2011, mullets were the 2nd most landed available information indicating that responding to episodic or changing fish in the Rio Grande do Sul artisanal current regulatory measures to protect environmental conditions. This can fisheries and the 5th most landed vulnerable species are poorly enforced, occur through a significant change or marine fish in all of Brazil. particularly within artisanal fisheries. loss of variation in life history Additionally, the artisanal gillnet Overall, the best available information characteristics (such as reproductive fisheries operating off Rio Grande do suggests heavy exploitation of R. fitness and fecundity), morphology, Sul are also known to bycatch and sell horkelli, particularly in the area where behavior, or other genetic pregnant females, mature males, and it was historically most abundant, and characteristics. Although it is unknown juvenile Brazilian guitarfish, despite its a significant lack of adequate regulatory if R. horkelli has experienced a loss of prohibited status. Based on the modeled mechanisms to protect the species from diversity, the significant reduction in exploitation scenarios and resultant overutilization throughout its range. population size on the Plataforma Sul, population growth rates described in the as well as the likely small populations Risk of Extinction demographic analysis above, continued elsewhere throughout its range, suggest Although there is significant fishing pressure by both artisanal the species may be at an increased risk uncertainty regarding the current fisheries targeting mullet, as well as of random genetic drift and could abundance of the species, the best other gillnet fisheries, and subsequent experience the fixing of recessive available information indicates that the fishery-related mortality of immature detrimental genes, reducing the overall species has suffered significant Brazilian guitarfish, is likely fitness of the species. historical population declines, with no contributing to the significant decline of indication that these trends have Threats Assessment the species and is a threat that places stabilized or reversed. Based on the Present threats to the species include the species at a high risk of extinction. species’ demographic risks, without overutilization by fisheries and In addition to the threat from artisanal adequate protection, these severely inadequate regulatory mechanisms. The fishing operations, juveniles and adults depleted populations are likely to be artisanal and industrial fisheries that of the species are also at risk of bycatch- strongly influenced by stochastic or historically contributed to the decline in related mortality by the industrial trawl depensatory processes. This R. horkelii are still active throughout the and gillnet fleets operating off Rio vulnerability is further exacerbated by species’ range and significantly Grande do Sul and Santa Catarina. the present threats of overutilization contribute to national marine fish These fleets focus trawling efforts on the and inadequacy of existing regulatory production. In fact, in Brazil in 2007, inner and outer continental shelf measures that continue to contribute to the industrial fleets were responsible for (between 29° S. and 34° S.), essentially the decline of the existing populations, landing over half of the marine fish from covering the entire seasonal adult compromising the species’ long-term the country’s South Region, where R. migratory corridor. Of concern is the viability. Therefore, based on the best horkelli is most concentrated, with fact that the R. horkelli catch from these available information and the above artisanal fisheries responsible for 10 industrial fleets are predominantly analysis, we conclude that the R. percent. The most recent statistics from juveniles, with estimates of juveniles horkelli is presently at a high risk of 2011 show that marine fish landings comprising around 76 to 94 percent of extinction throughout its range. from the South Region represent almost the landings from these fleets. Again, half of the fish production from that based on the modeled exploitation Protective Efforts region and 28.6 percent of the Brazilian scenarios, this level of juvenile catch is With the exception of the national total of marine fish landings. likely contributing to significant recommendations within Brazil and Because these artisanal and industrial declines in the population. Uruguay’s FAO NPOA-sharks plans fleets primarily operate in locations Additionally, the relatively recent discussed above, we were unable to find where R. horkelii would occur, and use expansion and operation of the Rio any other information on protective rather unselective fishing gear, their Grande do Sul and Itajai trawl fleets into efforts for the conservation of Brazilian operations are likely contributing previously unexplored depths of 100 m– guitarfish in Brazil, Uruguay, or significantly to the fishery-related 200 m on the outer shelf 28° S.–30° S., Argentina that would potentially alter mortality rates of the species and and the subsequent large catches of the extinction risk for the species. We impacting the status of the species. Brazilian guitarfish, also suggest that seek additional information on other Although trawl fishing in Brazil is areas that previously served as offshore conservation efforts in our public prohibited within 3 nm of the coast (<10 refugia for the Rio Grande do Sul comment process (see below).

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Proposed Determination uniform in size and are similar in adults Striped smoothhounds display clear Based on the best available scientific and juveniles (Heemstra 1997; Vooren ontogenetic (i.e., life-stage based) depth and commercial information as and Klippel 2005b; Rosa and Gadig distributions. In Rio Grande do Sul, presented in the status review report 2010). The first dorsal fin is short, neonates are common in inshore areas and this finding, we find that the broad, and triangular with a large base between Cassino Beach and Chuı´ in Brazilian guitarfish is presently in and is located closer to the pelvic fins depths less than 20 m, with the greatest danger of extinction throughout its than the pectoral fins (Compagno 1984; frequencies between 2 m–5 m depth range. We assessed the ESA section Rosa and Gadig 2010). The second from November to January (summer 4(a)(1) factors and conclude that the dorsal fin base is generally slightly months; Vooren and Klippel 2005b). As species faces ongoing threats from smaller than the first dorsal fin base, such, these shallow areas likely function overutilization and inadequacy of and a dermal ridge is present between as important nursery areas for the existing regulatory mechanisms the two fins (Vooren and Klippel species (Vasconcellos and Vooren 1991; throughout its range. The species’ 2005b). The pectoral and pelvic fins Soto 2001; Vooren and Klippel 2005b). natural biological vulnerability to have posterior margins that are nearly Adults are found mainly in water overexploitation and present straight, and the caudal fin is not well depths between 50 m–100 m in autumn developed, with a small and rounded and winter but move to shallower demographic risks (e.g., low and ≤ declining abundance, negative ventral lobe (Rosa and Gadig 2010). The depths ( 50 m) in spring and summer population growth rates, and likely striped smoothhound is grey or grey- (Vooren and Klippel 2005b). In the small and/or isolated populations at an brown on its dorsal side and white on summer, males are much more common increased risk of random genetic drift) its ventral side (Compagno 1984). at depths between 20 m and 50 m, and are currently exacerbating the negative Newborns and juveniles have dark bars are only rarely caught in waters less effects of the aforementioned threats, of irregular widths running across the than 20 m deep, whereas females can be placing this species in danger of dorsal surface of their head and body found in waters less than 20 m deep as extinction. We also found no evidence (Heemstra 1997). The distinguishing they move into coastal waters for of protective efforts for the conservation vertical bars are still present in adults, pupping during the summer months of Brazilian guitarfish that would reduce but are not nearly as defined as they are (Vooren and Klippel 2005b). Striped in juveniles (Sadowski 1977; Heemstra smoothhound are generally found in the level of extinction risk faced by the ° ° species. We therefore propose to list the 1997; Lorenz et al. 2010; Rosa and Gadig cooler water temperatures (11 C–15 C 2010). Overall, the striped smoothhound for juveniles during winter months, and Brazilian guitarfish as an endangered ° species. stands out from the other Mustelus >16 C for adults; Vooren and Klippel species in the southwestern Atlantic 2005b) and prefer water salinities Smoothhound Sharks because of its triangular dorsal and between 33.3 ppt and 33.6 ppt (Lopez Smoothhound sharks are members of pectoral fins, underdeveloped caudal Cazorla and Menni 1983). fin, unique tooth morphology, wide the family Triakidae and genus Diet and Feeding Mustelus. The Mustelus species are head, and small eyes (Rosa and Gadig often difficult to distinguish due to their 2010). Knowledge of the striped smoothhound’s diet is limited. Soto conserved morphology and highly Range and Habitat Use (2001) studied the stomach contents of variable intraspecific meristic The striped smoothhound is a 17 specimens captured off Parcel da characteristics. This problem is demersal shark species, found at depths Solida˜o in Rio Grande do Sul, Brazil. compounded in the southwestern between 1 m and 250 m along the Crustaceans were the most abundant Atlantic, with very few specimens, continental shelf and slope of the prey group, making up 82.4 percent of particularly of larger individuals, Southwestern Atlantic in Brazil, the diet, while fishes and mollusks were leading to a lack of comparative Uruguay, and Argentina (Soto 2001). present in lower numbers (11.8 percent ontogenetic observations that can be The species has a very restricted coastal and 5.9 percent, respectively). Box crabs used for species diagnosis (Rosa and distribution, ranging from Santa (Heptus pudibundus) were the most Gadig 2010). To date, there are at least Catarina in southern Brazil to Bahı´a prevalent crustacean, occurring in 52.9 five species of the genus Mustelus that Blanca in Buenos Aires Province, percent of the stomachs examined (Soto occur with overlapping ranges in the Argentina, which covers about 1,500 km 2001). southwestern Atlantic: M. canis, M. of coastline (Lopez Cazorla and Menni Growth and Reproduction higmani, M. norrisi, M. fasciatus and M. 1983; Vooren and Klippel 2005b; Lorenz schmitti (Rosa and Gadig 2010). Two of et al. 2010). During the winter, adult There is scant information on striped these species, M. fasciatus and M. biomass is concentrated on the smoothhound life history. Age and schmitti, are elasmobranchs that are Plataforma Sul between Rio Grande and growth studies are not available and being considered for listing in this Chuı´ off Rio Grande do Sul, Brazil conflicting data exist for sizes at birth finding. (Vooren 1997; Vooren and Klippel and maturity in Rio Grande do Sul. For Striped Smoothhound Shark (Mustelus 2005b). During the summer, a portion of example, one study reported that size at fasciatus) the population migrates from Brazil to birth is between 39 cm and 43 cm TL, Uruguay and Argentine waters, while and that sexual maturity is reached at Species Description the rest of the population remains on 130 cm and 135 cm TL for males and The striped smoothhound is one of the Plataforma Sul off Rio Grande do females, respectively (Vasconcellos and the most distinctive Mustelus species. Sul as year-round residents (Vooren Vooren 1991). More recent studies Its head is large, with very small eyes 1997; Vooren and Klippel 2005b). report smaller sizes, with birth and a sharply pointed snout (Compagno Outside of Brazil, the striped estimated between 35 cm and 38 cm TL 1984; Rosa and Gadig 2010). Labial folds smoothhound occurs only occasionally, and size at maturity estimated at 119 cm are present, and are longer on the upper with sporadic observations from the Mar TL for males and 121 cm TL for females jaw than on the lower jaw (Heemstra del Plata, Argentina, near the southern (Soto 2011; Vooren and Klippel 2005b). 1997; Rosa and Gadig 2010). The striped boundary of its range (Lopez Cazorla The smaller size at maturity seen in the smoothhound’s teeth are small and and Menni 1983). more recent studies could be a

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compensatory response to the high early 1970s and 1980s, and displayed Summary of Factors Affecting Striped levels of fishing mortality the species predictable abundance changes Smoothhound (Mustelus fasciatus) has experienced since the early 1980s throughout the year (Vooren 1997), they We reviewed the best available (see Overutilization for Commercial, are now considered sporadic in this area information regarding historical, Recreational, Scientific or Educational and rare in the northern and southern current, and potential threats to the Purposes section). The maximum portions of their range (Soto 2001). Prior striped smoothhound species. We find observed sizes for striped smoothhound to fisheries exploitation, it is thought that the main threat to this species is are 162 cm TL (17.5 kg) for males and that the striped smoothhound had overutilization for commercial 177 cm TL (29.7 kg) for females (Lorenz naturally low abundance based on their purposes. We consider the severity of et al. 2010). relatively low frequency of occurrence this threat to be exacerbated by the Striped smoothhound have placental in fishery research surveys (Vooren and species’ natural biological vulnerability viviparous reproduction (Vooren 1997) Klippel 2005b). For example, in to overexploitation, which has led to and a gestation period that lasts between research trawl surveys on the Plataforma significant declines in abundance of all 11 and 12 months (Soto 2001; Lorenz et life stages, particularly neonates. We al. 2010). Pregnant females migrate into Sul, conducted from 1972–2005 with find current regulatory measures shallow waters (<20 m) along the Rio over 1,500 hauls, striped smoothhound inadequate to protect the species from Grande do Sul coast to give birth from occurred at a frequency of only 10 further overutilization. Hence, we October to December (Vasconcellos and percent in the trawl hauls from the 10 identify these factors as additional Vooren 1991; Vooren 1997; Lorenz et al. m–100 m depth range (Vooren and threats contributing to the species’ risk 2010). Vooren and Klippel (2005b) Klippel 2005b) and comprised only 2 to of extinction. We summarize report that pupping takes place from 4 percent of the total elasmobranch information regarding these threats and November to January, but Soto (2001) CPUE for the period of 1980–1984. their interactions below according to the reports that it occurs earlier, from Despite this low frequency of factors specified in section 4(a)(1) of the September to November. Striped occurrence, Vooren and Klippel (2005b) ESA. Available information does not smoothhounds have 4–14 pups per note that neonates of the species were indicate that habitat destruction, litter, with an average of 8 pups relatively abundant in the 1980s in the modification or curtailment, disease, (Vasconcellos and Vooren 1991). summer and commonly observed along predation or other natural or manmade Newborns are seen in high frequency in the 10,688 km of the Rio Grande do Sul factors are operative threats on these November, along with females with coastline. In fact, for the period of 1981– species; therefore, we do not discuss mature follicles and postpartum uteri, 1985, estimated CPUE from artisanal these factors further in this finding. See suggesting an annual reproductive cycle fisheries operating off Rio Grande do Casselbury and Carlson (2015c) for (Vasconcellos and Vooren 1991). After Sul ranged from 1.9 individuals/haul for discussion of these ESA Section 4(a)(1) pupping, females move to deeper waters beach seines to 18.5 individuals/haul threat categories. to mate (Soto 2001; Vooren and Klippel for gillnet fishing gear. In research trawl 2005b; Lorenz et al. 2010). One study surveys conducted in shallow waters of Overutilization for Commercial, found a positive relationship of litter 10 m–20 m depths in 1981 and 1982, Recreational, Scientific, or Educational size and maternal size (Soto 2001); juvenile M. fasciatus occurred at a Purposes however, two other studies found no frequency of 54–86 percent in trawl The greatest threat to striped correlation (Vasconcellos and Vooren hauls with a CPUE of 2.55–3.95 kg/hour. smoothhound is overutilization in 1991; Heemstra 1997). However, in follow-up surveys commercial fisheries, particularly by Genetics and Population Structure conducted nearly two decades later, those fisheries operating on the Studies examining the genetics of the juveniles and neonates were mostly Plataforma Sul off Rio Grande do Sul. species or information on its population absent from hauls, despite significant The Plataforma Sul comprises structure could not be found. sampling in habitats where they had approximately one-third of the species’ been known to occur. In 2005, neonates geographic distribution and is the area Demography were noted as abundant along only 395 where the species was historically most The striped smoothhound is generally km of the Rio Grande do Sul coastline, concentrated. In fact, striped thought to have low fecundity, with a corresponding to an estimated 95 smoothhound were commonly caught as long gestation time (∼1 year), and an percent decline in occupied area by bycatch in the 1970s and 1980s on the average of only eight pups (range = 4– neonates between 1981 and 2005 Plataforma Sul in Brazil, albeit in low 14 pups). Information regarding natural (Vooren and Klippel 2005b). numbers (Soto 2001; Vooren and Klippel 2005b). Estimates of CPUE of M. mortality rates or the intrinsic rate of In Uruguay and Argentina, current population increase (r) of the striped fasciatus on the shelf in the early 1980s catches by fishermen are infrequent. varied between 2 kg/hr and 7 kg/hr (in smoothhound is unavailable; however, Additionally, trawl surveys conducted based on the life history parameters areas of low density) and 8 kg/hr to 33 along the coastal region of the described previously, the species likely kg/hr (in areas where the species was Bonaerensean (Buenos Aires) District of has low productivity, which may hinder more highly concentrated) (Vooren and northern Argentina and Uruguay its ability to recover from exploitation. Klippel 2005b). Although the presumed indicate a 96 percent decline in biomass naturally low abundance of striped Historical and Current Distribution and of the species between 1994 and 1999 smoothhound prohibited a directed Population Abundance (Hozbor et al. 2004). Striped fishery from developing for this species The striped smoothhound is smoothhounds were also absent from on the Plataforma Sul, they were and distributed from Santa Catarina in Argentine research surveys conducted continue to be caught as part of the southern Brazil to the Bahı´a Blanca in in the 1990s and are currently rarely multispecies smoothhound fisheries and Buenos Aires Province, Argentina. caught by the commercial fleet, as bycatch in fisheries for other species While striped smoothhound were once suggesting that the Argentine sea such as drums, flounders, and mullets considered a dominant permanent represents the periphery of its (Haimovici and Mendonc¸a 1996; Vooren resident in Rio Grande do Sul in the distribution (Massa 2013). and Klippel 2005b). Striped

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smoothhounds have been reported in 18.5 (individuals/set) and 75 percent, highest level of marine fish landings landings from the industrial pair and respectively, in 1981–1985 to 0.2 (121,960 t in 2011) (IBAMA/CEPERG double-rig trawl fleets, bottom longline (individuals/set) and 13 percent in 2012). Based on the trends in the and gillnet fleets and artisanal fisheries 2002–2003. In 2005, neonates remained available fishing data, it is unlikely that (Mazzoleni and Schwingel 1999). When common only in the inner edge of their the industrial and artisanal fishing on caught, large striped smoothhound former 10,688 km2 occupied area, in the Plataforma Sul, and particularly off weighing more than 4 kg are generally depths between 2 m–5 m: An area of the coast of Rio Grande do Sul within retained and those less than 4 kg are only 395 km2. This significant reduction striped smoothhound habitat, will discarded (Haimovici and Maceira in occupied area translates to an decrease in the foreseeable future, 1981), but the rate of discard mortality estimated 95 decline in neonate indicating that overutilization (in the is unknown. However, as both production and is likely a result of the form of bycatch mortality) is still a industrial and artisanal fishing intense artisanal and industrial fishing threat to the species. intensified on the Plataforma Sul in the pressure and overutilization of the Outside of Brazil, off Uruguay and 1980s and continued through the 1990s, species within this area. Trawl surveys Argentina, striped smoothhound are with the heavy use of trawls, gillnets conducted in the same area but in caught sporadically as bycatch in and beach seines within the habitat of depths of 10 m–20 m showed a similar gillnets, bottom longlines, and trawls in the striped smoothhound shark, the decline in the CPUE of juvenile striped fisheries targeting Brazilian flathead rates of fishery-related mortality smoothhounds, from 2.55 kg/hour in (Percophis brasiliensis), Argentinian experienced by the species clearly led to 1981 and 3.95 kg/hour in 1982 to 0.02 sandperch (Pseudopercis semifasciata), dramatic declines in its abundance kg/hour in 2005, an estimated 99 apron rays (Discopyge tschudii), striped (Soto 2001; Hozbor et al. 2004). percent decrease in abundance (Vooren weakfish (Cynoscion guatucupa) and whitemouth croaker (Micropogonias The intense coastal commercial and and Klippel 2005b). funieri) (Chiaramonte 1998; Lasta et al. artisanal fishing off Rio Grande do Sul In addition to the coastal artisanal and 1998; Domingo et al. 2008). Bycatch that takes place in nearshore waters industrial fisheries, the intense fishing levels and the associated fishery-related along the coast (see additional by the Plataforma Sul trawl fisheries mortality of striped smoothhound in discussion of these fisheries in the that operate between the coastal waters these fisheries have resulted in marked Brazilian guitarfish assessment) has and inner continental shelf (see declines in the population, with trawl likely had, and continues to have, the description of the pair trawl fleet in the surveys conducted in the coastal region greatest impact on the species. These Brazilian guitarfish assessment) also of the Bonaerensean District of northern coastal fisheries primarily use beach affected and continues to impact the Argentina and Uruguay indicating a 96 seines, gillnet and trawl gear in the reproductive capacity of the striped percent decline in the biomass of nearshore locations where striped smoothhound population in southern striped smoothhound between 1994 and smoothhound neonates and juveniles Brazil. These trawl fisheries, whose area 1999 (Hozbor et al. 2004). In the early are found year-round. This level of of operation intersects with the spring 2000s, annual landings of fishing effort exerts constant pressure on migration of female M. fasciatus, smoothhounds (primarily M. schmitti, the species before it reaches maturity incidentally catch both pregnant but also M. fasciatus and M. canis) in (Soto 2001; Vooren and Klippel 2005b), females and adult male striped Uruguay increased dramatically, from and consequently, affects the smoothhounds on the inner shelf fewer than 350 t in the 1990s to a peak recruitment of juvenile sharks into the (Haimovici and Mendonc¸a 1996; Vooren of 1,300 t in 2000 and remained above population (Vooren 1997). Significant and Klippel 2005b). As such, all life- 1,000 t through 2005; however, the declines in neonate and juvenile stages of the species as well as both cause for this reported increase in populations have already been sexes are subject to constant fishing landings is unknown and, since 2000, observed. Between the areas of Chuı´ and pressure year-round, which Vooren and landings have progressively declined Torres of Rio Grande do Sul, Brazil, for Klippel (2005b) point to as the primary (Domingo et al. 2008). In Uruguay’s example, neonates were abundant in the cause for the significant decline and latest 2013 Fishery Statistics Bulletin, summer in the 1980s, along the coast present rarity of the resident striped there were no reported landings of M. from depths of 2 m–20 m, representing smooth population on the Plataforma fasciatus (Direccio´n Nacional de an area of occupancy of about 10,688 Sul. As discussed in the Brazilian Recursos Acua´ticos (DINARA) 2014). km2. According to Hozbor et al. (2004), guitarfish assessment, fishing by the Similarly, in Argentina, striped gillnets set off beaches in this area industrial and artisanal fleets continues smoothhounds are also currently a rare would capture neonate striped to occur at high efforts on the occurrence (Casselberry and Carlson smoothhound in large numbers (10–100 Plataforma Sul and especially within 2015c). per set) in the 1980s; however, by 2003, the important coastal nursery and inner this level of removal had led to shelf habitats for the species (which Inadequacy of Existing Regulatory substantial declines in the population, overlap with R. horkelli). In fact, total Mechanisms with striped smoothhound currently marine fish landings from Rio Grande Like the daggernose shark and caught only sporadically and in much do Sul (where striped smoothhound are Brazilian guitarfish, the striped smaller numbers. Similarly, off of most concentrated on the Plataforma smoothhound is also listed as critically Cassino Beach (located close to the mid- Sul) have increased substantially in endangered under Annex I of Brazil’s point between Chuı´ and Torres) Vooren recent years, from 23,594 t in 2007 to endangered species list. Aside from and Klippel (2005b) estimated that 34,385 t in 2011 (an increase of 46 authorized conservation research CPUE of neonate striped smoothhound percent over 4 years) (MMA/IBAMA purposes, the capture, transport, storage, decreased by up to 99 percent in the 2007; IBAMA/CEPERG 2012). Out of the and handling of striped smoothhounds artisanal fisheries during this time 27 Brazilian States, Rio Grande do Sul is prohibited. There is also a prohibition period. Specifically, the CPUE of reports the 6th highest level of marine of trawl fishing within three nautical neonate striped smoothhound and fish landings and Santa Catarina (which miles of the coast of southern Brazil, frequency of its occurrence in the represents the northern periphery of the although the enforcement of this artisanal gillnet fishery sets went from species’ range in Brazil) reports the prohibition has been noted as difficult

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(Chiaramonte and Vooren 2007). In primarily from October to December), it characterized as sporadic and rare in addition, the species is still susceptible does little to decrease fisheries-related Uruguay and Argentina, respectively, to being caught as bycatch in the legally mortality of young striped survey data suggest that the migratory permitted coastal gillnet fisheries and smoothhounds which remain in these population has also experienced similar offshore trawl and gillnet fisheries and coastal waters following birth. In other declines. Based on trawl survey data vulnerable to the associated bycatch words, given that the depth distribution collected from along the Bonaerensean mortality (Lessa and Vooren 2007). of M. fasciatus extends from shallow District of northern Argentina and While the striped smoothhound is not coastal waters out to 100 m depths, and Uruguay, the population of striped listed as one of the 12 species of fishery records from Uruguay show that smoothhounds suffered an estimated 96 concern under Brazil’s FAO NPOA- the species is primarily bycaught in the percent decline in biomass between sharks, the plan does call for a fishing artisanal longline and gillnet fisheries 1994 and 1999. No other information on exclusion area over a large region of the (Domingo et al. 2008), this new abundance or trends was available from coast of Rio Grande do Sul at depths of resolution is unlikely to adequately this portion of the species’ range. 20 m to protect nursery areas (which decrease the threat of overutilization to However, considering the species was of would include the striped smoothhound striped smoothhounds. naturally low abundance prior to nursery habitat) (Lessa et al. 2005). The exploitation, and fishing pressure has Extinction Risk plan also proposes a fishing closure historically been high (particularly on between 32° S. and 34° S., where adults The best available information neonates in nursery areas and juvenile of the species now seem to be found in provides multiple lines of evidence and adults on the inner shelf, including greatest abundance (Vooren and Klippel indicating that the M. fasciatus on both the resident and migratory 2005b). However, as mentioned currently faces a high risk of extinction. populations) with no indications that previously, the plan was only just Below, we present the demographic risk this pressure has ceased, it is likely that approved as of December 2014, and will analysis, threats assessment, and overall the species has continued to suffer not be fully implemented for another 5 risk of extinction for the striped declines throughout its range. years. Thus, the implementation and smoothhound shark. Growth Rate/Productivity effectiveness of the recommendations Demographic Risk Analysis outlined in the plan remain uncertain, Very little information is known about the life history of M. fasciatus. Age and with the best available information Abundance growth studies are unavailable for the indicating that current regulatory While there are no quantitative species, and there is conflicting measures in Brazil to protect vulnerable abundance estimates available for M. information reported from the literature species are poorly enforced. fasciatus, qualitative information and regarding the species’ size at birth and In contrast to Brazil, Uruguay’s FAO historical catch data can provide some size at maturity from Rio Grande do Sul, NPOA-sharks does list the striped insight into the current abundance of Brazil. Estimates of size at maturity smoothhound as a species of high the species. Based on data from research range from 119 to 130 cm TL for males priority (Domingo et al. 2008), and, as trawl surveys, it is thought that the and 121 to 135 cm TL for females, with stated previously, has set goals to collect striped smoothhound naturally occurred the smaller and more recent size the necessary information on its priority at low abundance before they were estimates a possible compensatory species in order to conduct abundance exploited in fisheries (Vooren and response to fishing mortality. Size at assessments, review current fishing Klippel 2005b), and were once birth ranges from 35 to 48 cm TL. The licenses, and promote public awareness considered a dominant permanent species is generally thought to have low to release captured individuals. resident species on the Plataforma Sul. fecundity, with a long gestation time (∼1 However, no updated results from the However, presently, the species is rarely year) and an average of only 8 pups per goals and priorities of this plan could be observed anywhere in its range and litter. These reproductive characteristics found. As such, their implementation caught only sporadically. Historical data suggest the species has relatively low and overall effectiveness at decreasing from artisanal gillnet and beach seine productivity, similar to other the threats to the striped smoothhound fisheries suggest neonate production on elasmobranch species, which has likely remains highly uncertain. Additionally, the Plataforma Sul has decreased by 95 hindered its ability to quickly rebound in 2013, the National Directorate of percent since the 1980s. Additionally, from threats that decrease its abundance Aquatic Resources (DINARA), the state research trawl survey data estimate a (such as overutilization). agency responsible for regulating and decline in juvenile striped controlling fishing and aquaculture in smoothhounds in these coastal waters of Spatial Structure/Connectivity Uruguay, passed a resolution around 99 percent over this same The striped smoothhound has a very authorizing fishing with gillnets and period. Considering adult female striped restricted coastal range of only 1,500 longlines in the Rio de la Plata and smoothhounds follow a spring km. On the Plataforma Sul off southern Atlantic Ocean at a distance less than migration into these same coastal areas Brazil, there is thought to be a 300 m from the coast, between March 1 for pupping purposes, and, thus, are permanent, year-round resident and October 31 of each year. This type also susceptible to these artisanal population. Vooren and Klippel (2005b) of fishing was previously prohibited in fisheries, the significant declines in note that the area occupied by this 2008; however, due to concerns brought neonate and juvenile abundance likely population represents one third of the forth by the artisanal fishermen, correspond to declines in the number of species’ total range, and that the primarily of the socio-economic nature, reproductively active females in the conservation of this resident population DINARA revised the prohibition to population as well, as overutilization of is integral to the conservation of the allow for this seasonal fishing the species through the direct removal taxon as a whole, indicating the relative (Resolution No. 24/04/2013 MGAP). of young striped smoothhound shark importance of this population to the Although this seasonal restriction recruits. species’ survival. However, there is also should provide some protection for the Although CPUE data are lacking from thought to be a migratory population population of migrating pupping other parts of the species’ range, with that is present on the Plataforma Sul in females (which moves inshore to pup catches of striped smoothhound the winter that returns to Uruguay and

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Argentina in the summer concurrent coastal waters provide strong evidence information indicates that the species with changes in water temperature. No that a 95 percent reduction in annual has suffered significant declines information exists on the connectivity production of neonates occurred from throughout its range due to between the resident and winter migrant 1984 to 2005 as a result of constant overutilization in industrial and M. fasciatus populations found on the fishing pressure in important coastal artisanal fisheries. The species’ very Plataforma Sul; however, based on the nursery areas. Adult striped restricted coastal range, with data to significant decline of the population off smoothhounds are also susceptible to suggest it has undergone a decline of the Buenos Aires Province, it seems these fisheries during their spring over 90 percent in one third of this likely that the increased fishing pressure migration into these same coastal areas range, combined with its present rarity on the migratory population while they for pupping, and are at risk of being throughout the rest of its range, make it winter on the Plataforma Sul may be caught as bycatch by the industrial particularly susceptible to local negatively impacting the populations gillnet and trawl fleets operating on the extirpations and significantly increases found in other parts of the species’ inner shelf throughout the rest of year. its risk of extinction from environmental range. In fact, the level of fishing mortality on and anthropogenic perturbations or the migratory wintering population on catastrophic events. With no indication Diversity the Plataforma Sul may have led to the that abundance trends have stabilized or The loss of diversity can increase a observed declines in the striped reversed in recent years, nor any species’ extinction risk through smoothhound population found off the indication that regulatory measures decreasing a species’ capability of coast of northern Argentina. Thus, the have been implemented or are responding to episodic or changing intense fishing effort by the commercial adequately enforced to protect the environmental conditions. This can and artisanal fisheries on the Plataforma Plataforma Sul neonates in important occur through a significant change or Sul appear to be negatively affecting the nursery areas, the local reproducing loss of variation in life history reproductive capacity and growth of the adult population, or the migratory characteristics (such as reproductive population throughout its range. population from unsustainable fishing fitness and fecundity), morphology, In 2004, the species was listed on mortality levels, it is likely that the behavior, or other genetic Brazil’s endangered species list, which species continues to suffer from characteristics. Although it is unknown effectively prohibited the capture of this population declines. Based on the if M. fasciatus has experienced a loss of species. As of 2014, the species was species’ demographic risks, these diversity, high fishing pressure on classified as ‘‘critically endangered’’ on severely depleted populations are likely neonates and reproductively active this list. Although the species is not to be strongly influenced by stochastic adults in coastal waters has negatively identified as one of 12 species of or depensatory processes without affected recruitment rates of neonates concern under Brazil’s FAO NPOA- adequate protection. This vulnerability into the population, resulting in a sharks, the plan calls for fishing is further exacerbated by the present significant depletion of the resident closures in areas of <20 m deep that threats of overutilization and population on the Plataforma Sul. This would provide protection to neonates inadequacy of existing regulatory reduction of the important resident and juveniles, as well as other closures measures that continue to contribute to population in Brazil, combined with the to protect adult aggregations. In the decline of the existing populations, likely small populations elsewhere Uruguay, the striped smoothhound is compromising the species’ long-term throughout its range, suggest the species listed as a species of high priority on its viability. Therefore, based on the best may be at an increased risk of random FAO NPOA-sharks (Domingo et al. available information and the above genetic drift and could experience the 2008); however, as mentioned analysis, we conclude that M. fasciatus fixing of recessive detrimental genes, previously, the implementation and is presently at a high risk of extinction reducing the overall fitness of the effectiveness of the recommendations throughout its range. species. outlined in both the Brazilian and Protective Efforts Threats Assessment Uruguayan plans remain uncertain, with the best available information indicating With the exception of the The primary threat to striped that current regulatory measures in both recommendations within Brazil and smoothhounds is overutilization in countries are inadequate to protect the Uruguay’s FAO NPOA-sharks, we were commercial fisheries. Although not species from further overutilization. unable to find any other information on targeted in any fisheries throughout its Given the continued and significant protective efforts for the conservation of range, due to its presumed naturally low fishing effort by the industrial trawl striped smoothhound sharks in Brazil, abundance, striped smoothhounds are fleet and artisanal gillnet on the Uruguay, or Argentina that would caught as part of the multispecies Plataforma Sul, contributing to the potentially alter the extinction risk for smoothhound fisheries and as bycatch fishing mortality of the resident the species. We seek additional in fisheries for other species such as population as well as the wintering information on other conservation drums, flounders, and mullets. While migratory population, and inadequacy efforts in our public comment process adult striped smoothhounds were once of existing regulatory measures to (see below). commonly caught as bycatch in the control the exploitation of the marine Proposed Determination 1970s and 1980s in Brazil, albeit in low resources throughout the species’ range, numbers, they are now considered rare the best available information suggests Based on the best available scientific in commercial catches. Additionally, that overutilization of the species by and commercial information as intensive fishing by gillnet and trawl industrial and artisanal fisheries is a presented in the status review report fisheries in shallow coastal areas where threat significantly contributing to its and this finding, we find that the striped juveniles and neonates occur results in risk of extinction. smoothhound is presently in danger of constant fishing pressure on the species extinction throughout its range. We before it reaches maturity, negatively Risk of Extinction assessed the ESA section 4(a)(1) factors affecting recruitment of neonates into Although there is significant and conclude that the species faces the population. In fact, the historical uncertainty regarding the current status ongoing threats from overutilization and data on the abundance of newborns in of the species, the best available inadequacy of existing regulatory

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mechanisms throughout its range. The smoothhound is found in waters with fishes, isopods, and polychaetes, and, to species’ natural biological vulnerability surface temperatures of 8 °C–11.7 °C a lesser extent, some teleosts and to overexploitation and present and bottom temperatures of 5.5 °C–11 °C cephalopods (Chiaramonte and demographic risks (e.g., significantly (Menni 1985; Chiaramonte and Pettovello 2000; Van der Molen and reduced and declining abundance Pettovello 2000) and salinity that is Caille 2001). levels, decreases in neonate production generally 22.4 practical salinity units and recruitment, low productivity, (psu) and higher (Molina and Cazorla Growth and Reproduction restricted range with likely small and/or 2011). The narrownose smoothhound has an Like striped smoothhounds, a portion isolated populations at an increased risk estimated lifespan of 20.8 and 24.7 years of the narrownose smoothhound of random genetic drift) are currently for males and females, respectively population is migratory. In the winter, exacerbating the negative effects of the (Hozbor et al. 2010). In general, aforementioned threats, placing this juveniles, adults, and gravid females migrate north into Brazilian waters and narrownose smoothhound females grow species in danger of extinction. We also faster and grow to a larger size than found no evidence of protective efforts remain there from April to November (Haimovici 1997; Vooren 1997; Oddone males (Chiaramonte and Pettovello for the conservation of striped 2000; Sidders et al. 2005; Segura and smoothhound that would reduce the et al. 2005; Massa et al. 2006). This migration is thought to be triggered by Milessi 2009). Maximum recorded size level of extinction risk faced by the for M. schmitti is 110 cm TL, with a species or otherwise alter its current cold water moving north into their Argentinian range (Haimovici 1997). modal TL in Brazil of 60 cm for males status. We therefore propose to list the and 72 cm for females ((Massa et al. striped smoothhound shark as an Water temperatures in the wintering ° 2006; Molina and Cazorla 2011). Size at endangered species. grounds are usually between 12 C and 20 °C (Massa et al. 2006). In the spring, maturity varies throughout the Narrownose Smoothhound Shark summer, and autumn (December to narrownose smoothhound’s range, with (Mustelus schmitti) April) narrownose smoothhounds are estimates for male size at 50 percent maturity ranging from 55 cm TL to 59 Species Description most common in waters off Uruguay (Vooren 1997; Oddone et al. 2005) and cm TL and for females ranging from 56 The narrownose smoothhound shark Argentina, with highest abundance in to 72 cm TL (Chiaramonte and has a slender body, similar in form to Argentinian waters noted off Buenos Pettovello 2000; Oddone et al. 2005; other triakids, and a short head Aires Province and northern Patagonia Segura and Milessi 2009; Colautti et al. (Compagno 1984; Rosa and Gadig 2010). (Molina and Cazorla 2011). 2010). Age at first breeding in Brazil is The species has large eyes and a snout 4 years for females and 3 years for that is bluntly angular (Compagno 1984) Diet and Feeding males, while it is 6.5 years for females with a narrow internostril distance Olivier et al. (1968) first characterized and 5.7 years for males in Argentina (Rosa and Gadig 2010). Like M. the diet of the narrownose (Casselberry and Carlson 2015d). fasciatus, labial folds are present on the smoothhound as carcinophagous (i.e., Narrownose smoothhound sharks are mouth and are longer on the upper jaw eats crabs and other crustaceans), non-placental and reported to be yolk- than on the lower jaw (Compagno 1984; benthic infaunal (i.e., eats animals that sac viviparous (Hamlett et al. 2005; Heemstra 1997; Rosa and Gadig 2010). live in the substrate), and ´ Narrownose smoothhounds are grey ichthiophagous (i.e., eats fish). The Galındez et al. 2010). Their with numerous small white spots on narrownose smoothhound is an reproductive cycle is annual with a their dorsal side and solid white opportunistic predator that generally gestation of 11 months followed by coloration on their ventral side feeds on epifaunal benthic organisms immediate ovulation and mating (Compagno 1984; Heemstra 1997). The and the diet appears to vary (Chiaramonte and Pettovello 2000). In trailing edges of both dorsal fins have geographically and ontogenetically the spring, females move inshore to pup exposed ceratotrichia (slender soft or (Capitoli et al. 1995). For example, in and mate, and then migrate offshore in stiff filaments of an elastic protein that Rı´o de la Plata and El Rinco´n, late summer to early autumn (Colautti et superficially resembles keratin), a Argentina, the diet is generally al. 2010). Reproduction occurs at distinctive characteristic for the species dominated by crustaceans, fishes, and different times, ranging from late (Rosa and Gadig 2010). The pectoral and polychaetes; however, as narrownose November in northern Argentina to mid- pelvic fins are both relatively small, smoothhounds increase in body size, December at the southern extent of its (Compagno 1984) and the ventral lobe of the consumption of polychaetes range (Molina and Cazorla 2011). Litter the caudal fin is poorly developed declines and is replaced by more fishes size varies between 2 and 14 pups (Heemstra 1997). and crustaceans. The shift to (Massa et al. 2006), with an average crustaceans occurs around 60 cm TL, litter size of around 4 to 5 pups (Sidders Range and Habitat Use while narrownose smoothhounds et al. 2005; Galı´ndez et al. 2010). Litter The narrownose smoothhound is around 85 cm TL feed primarily on fish size increases significantly with found in the southwestern Atlantic from (Belleggia et al. 2012). Temporal and maternal length (Oddone et al. 2005; southern Brazil to southern Argentina ontogenetic variations in diet were also Corte´s 2007), but larger females do not between 22° S. and 47°45′ S. (Belleggia found for M. schmitti in Anegada Bay, produce larger offspring (Sidders et al. et al. 2012). Rio de Janeiro, Brazil, is the Argentina, where neonates are more 2005). Nursery grounds for the northernmost limit of the species’ range specialized feeders and predominantly narrownose smoothhound shark in (Oddone et al. 2007) and Rı´a Deseado, consume decapods, and adults more Argentina (based on higher abundance Argentina is the southernmost limit commonly consume polychaetes, of neonates and juveniles within these (Chiaramonte and Pettovello 2000). decapods, bivalves, and occasionally areas) are found in the El Rinco´n area Narrownose smoothhound occurs at cephalopods (Molina and Carzorla (including Bahı´a Blanca and Anegada depths up to 120 m in Argentina and 2011). Smaller scale diet studies in Bay) and the Rı´o de la Plata (including has been captured as deep as 195 m in Argentina also found the diet to be Samborombo´n Bay) (Chiaramonte and Brazil (Belleggia et al. 2012). In dominated by epifaunal benthic Pettovello 2000; Molina and Cazorla Argentinian waters, narrownose organisms, including decapod crabs, 2011).

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Genetics and Population Structure off Rio de la Plata as high as 44 t/nm2 protect the species from further In terms of population structure, only in 1994 (Cousseau et al. 1998). overutilization. Hence, we identify these one genetics study has been conducted Throughout the rest of the Argentine- factors as additional threats contributing to determine if multiple stocks occur Uruguayan Common Fishing Zone to the species’ risk of extinction. We throughout the species’ range (Pereya et (AUCFZ) [an area that extends 200 nm summarize information regarding these threats and their interactions below al. 2010). Results of this study indicate off the coast from the border of Uruguay and Brazil to just south of Necochea, according to the factors specified in that M. schmitti comprises a single Argentina)] densities of narrownose section 4(a)(1) of the ESA. Available demographic unit in the Rı´o de la Plata smoothhounds ranged between 1 and 10 information does not indicate that area and its maritime front (area t/nm2, with some areas supporting habitat destruction or modification, separating Uruguay and Argentina), densities as high as 22 t/nm2 (Cousseau disease, predation or other natural or suggesting high connectivity and genetic et al. 1998). Based on data from research manmade factors are operative threats homogeneity over this geographic range surveys conducted in the spring in on these species; therefore, we do not (Perey et al. 2010). The authors attribute Argentine maritime waters (covering discuss these factors further in this this genetic homogeneity to the likely coastal Buenos Aires and waters off finding. See Casselbury and Carlson high dispersal and migration rates of the Uruguay from 35° S.–41° S.), abundance (2015d) for discussion of these ESA species (based on tagging studies of of M. schmitti in this area increased section 4(a)(1) threat categories. related species M. antarcticus and M. from 82,000 t in 1978 to 184,302 t in Overutilization for Commercial, lenticulatis; Francis 1988) and lack of 1994. In 1999, M. schmitti abundance on Recreational, Scientific, or Educational obvious dispersal barriers in the study the continental shelf and slope from 34° Purposes area. The study also found that S.–48° S. was estimated to be 191,722 t nucleotide diversity in M. schmitti was (Argentina FAO NPOA-sharks 2009). The primary threat to the narrownose lower than that reported for other Although recent abundance estimates smoothhound is overutilization in elasmobranchs. These results may could not be found, Massa et al. (2006), commercial and artisanal fisheries as indicate that narrownose smoothhound citing unpublished data, indicate that the species is intensely fished experienced a genetic bottleneck, recent between 1998 and 2002, biomass of the throughout its entire range, including expansion, or selection, which species declined by 22 percent in main within its nursery grounds. In potentially occurred during the fishing areas along the coast of Buenos Argentina, M. schmitti is considered the Pleistocene Era (Pereyra et al. 2010). Aires Province (Argentina) and the most important elasmobranch in Demography Bonaerensean region (Uruguay) and Argentine fisheries, making up 9–12 national landings in Argentina percent of the total landings from The annual population growth rate for decreased by 30 percent. By 2003, coastal fleets (Galı´ndez et al. 2010), and narrownose smoothhound in Brazil was abundance of M. schmitti (between 35° is the most heavily exploited shark calculated to be 1.058 between 1980 and S.–41° S.) had fallen to 88,500 t species in artisanal fisheries. As bycatch 1994 (Massa et al. 2006). More recently, (Argentina FAO NPOA-sharks 2009). in Argentine commercial bottom trawls, using life history parameters from Declines in abundance continued to be narrownose smoothhounds comprise individuals collected off Mar del Plata, seen in Argentine waters through 2005 around 20 percent of the coastal harvest Argentina, Corte´s (2007) determined the (Massa and Hozbor 2008). Similarly, in from these fisheries (Colautti et al. intrinsic rate of increase (r) for Brazil, based on CPUE data, abundance 2010). In the 1990s, fishing for the narrownose smoothhound to be 0.175 of the winter migrant population of M. species increased in the directed per year when the population is not schmitti is estimated to have declined industrial shark fisheries (Massa et al. subject to exploitation (lower 95 percent by 85 percent between 1985 and 1994 2004a), with the narrownose confidence limit = 0.030; upper 95 (Miranda and Vooren 2003), and Massa smoothhound being the main shark percent confidence limit = 0.314). et al. (2006) note that a small local caught in the Argentine Sea (based on Because of this relatively high intrinsic breeding population that was relatively an extracted biomass of 10,200 t for that rate of increase, Corte´s (2007) concluded common in the 1980s in southern Brazil time period), and the second most that narrownose smoothhound could has seemingly been extirpated from the consumed domestic fish (Van der Molen withstand higher levels of exploitation area. et al. 1998; Chiaramonte 1998). Between than other coastal sharks in the Buenos 1981 and 1991, commercial catches of Aires coastal region, with sustainable Summary of Factors Affecting M. schmitti ranged from 5,000 t–8,000 t, exploitation rates equivalent to an Narrownose Smoothhound (Mustelus with peak landings of 13,000 t in 1988 annual removal rate of about 10 percent schmitti) (Cousseau and Perrotta 2000 cited in of the population. Natural mortality We reviewed the best available Massa et al. 2004a; FAO Global Capture rates of the species ranged from 0.139 to information regarding historical, Production Database). From 1992 to 0.412 (Corte´s 2007). These demographic current, and potential threats to the 1997, total catch of narrownose parameters place narrownose narrownose smoothhound shark. We smoothhound remained fairly stable, smoothhound toward the faster growing find that the main threat to this species hovering between 6,000 t and 8,000 t end of the ‘‘fast-slow’’ continuum of is overutilization for commercial (Massa et al. 2004a), whereas the population parameters calculated by purposes. We consider the severity of number of Argentine fishing vessels Corte´s (2002), which means this species this threat to be reduced by the species’ catching M. schmitti increased from 216 generally has a higher potential to natural biological ability to withstand to 298 (Massa and Hozbor 2003). This recover from exploitation. higher levels of exploitation. However, increase in vessels and associated we find that historical and present fishing pressure on the species Historical and Current Distribution and levels of utilization have exceeded the consequently led to significant declines Population Abundance species’ biological capacity to quickly in the abundance of the species off the The narrownose smoothhound is the recover from exploitation, and have Argentine coast over this time period. most abundant and widely distributed subsequently led to significant declines Specifically, between 1992 and 1998, triakid in the Argentine Sea (Van der in abundance. We also find that current CPUE declined by 50 percent for the Molen and Caille 2001), with densities regulatory measures are inadequate to fishing fleet comprised of small-sized

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

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since 2008, total landings of M. schmitti abundant in the 1980s have since which did little to protect the M. reported by Argentina and Uruguay to seemingly disappeared, with data that schmitti population from fishing the FAO have decreased by over 57 show an absence of neonate individuals mortality as a smoothhound fishery percent and 63 percent, respectively, from artisanal beach net catches in 2003 operated within the bay waters. although no corresponding effort and coastal trawl surveys conducted in However, in 2004 and 2008, fishing was information is available. Despite the 2005 (Vooren et al. 2005b). Further, banned in the bay due to concern over multiple indicators of overutilization of Massa et al. (2006) report that a small the conservation of the bay’s natural the species, in 2013, Argentina landed local population of narrownose resources, and since 2008, the a total of 4,379 t of M. schmitti and smoothhounds that was known to give smoothhound fishery in Anegada Bay Uruguay landed 194 t (FAO Global birth in south Brazil in November and has remained closed (Colautti et al. Capture Production Database), remain through February may have been 2010). However, as Anegada Bay is suggesting the species is still considered extirpated, but additional information to surrounded by the larger El Rinco´n area, valuable catch and bycatch in these confirm this potential extirpation is which also includes a number of other countries. unavailable. nursery habitats for the species and is In Brazil, M. schmitti occurs as winter As discussed in both the Brazilian open to fishing, it is unclear how migrants on the Plataforma Sul off Rio guitarfish and striped smoothhound effective the protections in Anegada Bay Grande do Sul and, similar to R. horkelli assessments, fishing by the industrial will be in decreasing the extinction risk and M. fasciatus, is caught by the trawl and artisanal fleets continues to occur at of the species from overutilization. and oceanic gillnet fleets operating on high efforts on the Plataforma Sul, and While these specific areas provide the continental shelf. From 1975 to especially within the important coastal important protection for the species 1997, M. schmitti was one of two nursery and inner shelf habitats for the during critical life stages, they comprise species that made up the majority of species (which overlap with both R. a very small portion of the species’ demersal shark landings in the port of horkelli and M. fasciatus). This heavy range and it is unclear to what extent Rio Grande (the other being the school fishing pressure may have led to the the species relies on these small nursery shark, Galeorhinus galeus; Miranda and apparent extirpation of the local areas for recruitment to the population. Vooren 2003). Targeted fishing for the breeding population of narrownose In Uruguay, regulations that likely species is thought to have increased smoothhound in southern Brazil (Massa contribute to decreasing the fishery- from the mid 1970s through the 1980s, et al. 2006 citing Vooren and Lamo´naca related mortality of the species include as evidenced by the near tripling of unpublished data) and is likely a summer trawling ban in 25 m to 50 m CPUE values of M. schmitti in the single contributing to the fishing mortality of depths between La Paloma and Chuy trawl fleet, from 2.48 t/trip in 1975 to the wintering migratory population. and specific fishery area closures in the 7.31 t/trip in 1987 (Miranda and Vooren Based on the trends from available spring, summer, and autumn on the 2003). Likewise, the CPUE of M. fisheries data (see R. horkelli and M. Uruguayan continental shelf, designated schmitti by pair trawls from 1975 to fasciatus assessments), it is unlikely that to protect juvenile hake (Merluccius 1987 reflected a similar trend, the industrial and artisanal fishing on hubbsi) but which also correspond with increasing from 0.35 t/trip to 2 t/trip the Plataforma Sul, and particularly off high use areas of the narrownose (Miranda and Vooren 2003). However, the coast of Rio Grande do Sul within smoothhound population (Pereyra et al. CPUE values for both fleets decreased narrownose smoothhound habitat, will 2008). rapidly after 1987, with values in 1994 decrease in the foreseeable future, Both Argentina and Uruguay list the (1 t/trip for single trawl and 0.3 t/trip for indicating that overutilization (in the narrownose smoothhound as a high pair trawl) indicating an approximate 85 form of bycatch mortality) will continue priority species within their respective percent decline in abundance of M. to be a threat to the species leading to FAO NPOA-sharks (Domingo et al. schmitti from 1985 numbers (Miranda further declines in the wintering 2008; Argentina FAO NPOA-sharks and Vooren 2003). Despite the decline, migratory population. 2009). These plans, as stated previously, M. schmitti was still being landed at the set goals to collect the necessary Inadequacy of Existing Regulatory port of Rio Grande from April to information on its priority species in Mechanisms October in 1994 and 1995 by single order to conduct abundance trawl and oceanic gillnet fleets, with In Argentina, there are few regulations assessments, increase research and peak CPUE from these fleets in place to protect narrownose improve management of the species, corresponding with the seasonal smoothhound nursery habitat. For review current fishing licenses, and occurrence of the species on the example, Rı´a Deseado (∼40 km; 47°45′ promote public awareness to release Plataforma Sul. S.; 65°55′ W.), the southernmost limit of captured individuals. However, no Similar to the trends seen in the the narrownose smoothhound’s range, is updated results from the goals and striped smoothhound within the coastal designated as a nature preserve and priorities of these plans could be found. waters off southern Brazil, neonates of protects the local population from As such, the implementation and M. schmitti have also declined in fishery-related mortality (Chiaramonte overall effectiveness of these plans at abundance, a likely result of the intense and Pettovello 2000). It has been decreasing the threats to the narrownose coastal commercial and artisanal fishing identified as a nursery area, where smoothhound remains highly uncertain. along the Brazilian coast (see additional breeding adults, neonates, and juveniles In the AUCFZ, the area where current discussion of these fisheries in the enter Rı´a Deseado waters in the late fisheries information indicates assessments for Brazilian guitarfish and spring and stay until late summer narrownose smoothhounds may likely striped smoothhound). As mentioned (Chiaramonte and Pettovello 2000). be most abundant and heavily targeted, previously, these coastal fisheries Anegada Bay (39°50′51″ S. to 40°43′08″ the Comisio´n Te´cnica Mixta del Frente primarily use beach seines, gillnet and S. and 62°28′44″ W. to 62°03′00″ W.), Marı´timo (CTMFM) is in charge of trawl gear in the nearshore locations off Argentina, another known narrownose managing fish stocks and does so Rio Grande do Sul, habitat for smoothhound nursery area, is also through the implementation of catch narrownose smoothhound neonates and protected from fishing operations. The limits and fishery closures. For juveniles. Consequently, neonate M. bay was previously designated as a example, every year, the CTMFM schmitti populations that were once multiple use zone reserve in 2000, implements a prohibition against

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demersal trawling in an area that covers which requires a special license from 2002, biomass of M. schmitti reportedly a large section of the common fishing IBAMA. There is also a prohibition of declined in the main fishing areas along zone, extending across the continental trawl fishing within three nautical miles the coast of Buenos Aires Province and shelf, in order to protect vulnerable from the coast of southern Brazil, the surrounding region by chondrichthyans from fishery-related although the enforcement of this approximately 22 percent (Massa et al. mortality. This prohibition, which is prohibition has been noted as difficult 2006). National landings also decreased usually in place between November and (Chiaramonte and Vooren 2007). In in Argentina by 30 percent during this March, helps to decrease fishery-related addition, the species is still susceptible same time period and have continued to mortality of the narrownose to being caught as bycatch in the legally decline based on FAO landings data smoothhound shark during at least part permitted coastal gillnet fisheries and through 2013. It is important to note of the year. The CTMFM also establishes offshore trawl and gillnet fisheries and that the decrease in landings is not due additional area closures to trawling gear vulnerable to the associated bycatch to falling market values as M. schmitti throughout the year in the AUCFZ, mortality (Lessa and Vooren 2007). continues to fetch a high price in the including within the Rio de la Plata Additionally, unlike the striped Argentine domestic market (Massa et al. (where historical estimates of smoothhound, the narrownose 2004b). In 2003, the spring time narrownose smoothhound were as high smoothhound is listed as one of the 12 abundance of M. schmitti from coastal as 44 t/nm2; Cousseau et al. 1998), in species of concern under Brazil’s FAO Buenos Aires and Uruguay (between 34° order to protect whitemouth croaker NPOA-sharks and would also benefit S.–41° S.) was estimated to be 88,500 t, (Micropogonias furnieri) and juvenile from the proposed fishing closures and which represents a 50 percent and 39 hake from overexploitation by the other management measures outlined in percent decline from estimated values fisheries. As these areas correspond the plan. However, as mentioned in 1994 and 1999, respectively (Massa et with high use by the narrownose previously, the plan was only just al. 2004a). Additionally, based on smoothhound population, the trawling approved as of December 2014, and will estimates calculated in 2007, size at bans will also directly help to protect not be fully implemented for another 5 maturity of the species has the narrownose smoothhound from years. Thus, the implementation and chronologically decreased since the additional fishery-related mortality. effectiveness of the recommendations 1970s, a strong indication of In terms of the direct management of outlined in the plan remain uncertain, overutilization of the species and M. schmitti sharks, from 2002 to 2010, with the best available information declining abundance. the CTMFM has set the total permissible indicating that current regulatory In Uruguay, there is conflicting catch limit for all Mustelus spp. at 4,850 measures in Brazil to protect vulnerable information regarding the trend in t. In 2011, this limit was lowered to species are poorly enforced. catches of M. schmitti. Landings of 4,000 t (Res. N° 5/11, Res. N° 5/02), and smoothhounds in Uruguay are in 2012, the CTMFM set a species- Extinction Risk aggregated at the genus level because specific total permissible catch limit for The best available information catch is often reported by common narrownose smoothhound at 4,500 t provides multiple lines of evidence name and the same common name is ° ° (Res. N 11/13, Res. N 9/12). This catch indicating that the M. schmitti currently used for multiple species. Thus, limit remained at this level until 2015, faces a moderate risk of extinction. identifying the true species composition ° when it was reduced to 3,500 t (Res N Below, we present the demographic risk of shark catches in Uruguay is 6/15). However, despite these maximum analysis, threats assessment, and overall problematic. According to Domingo et allowable catch levels for Mustelus spp. risk of extinction for the narrownose al. (2008), landings of smoothhounds in that have been set since 2002, smoothhound shark. Uruguay (primarily M. schmitti) McCormack et al. (2007) reports that increased dramatically between 1999 elasmobranch quotas and size Demographic Risk Analysis and 2000, reaching 1,300 tons, and then regulations are largely ignored in Abundance steadily declined to approximately 850 Argentina and poorly enforced. This tons by 2005. Based on landings data may explain why population declines There is limited information available reported to the FAO, catches of M. continued to occur in this part of the regarding quantitative abundance schmitti have continued to decline, with species’ range even after regulations estimates of narrownose smoothhound only 194 t reported in 2013. However, were implemented to sustainably throughout its range. However, biomass without corresponding effort manage the species. Due to a lack of estimates as well as trends in information, it is unclear if the decrease abundance data since 2003, it is unclear commercial landings and CPUE data can in landings is a result of decreases in whether the catch limits for Mustelus provide some insight into the abundance in the species. spp. have positively affected the abundance of the species. The In Brazil, M. schmitti occurs as winter population since 2002, though it is narrownose smoothhound is the most migrants on the Plataforma Sul and is worth noting that since 2010, catches of abundant and widely distributed triakid caught by the trawl and oceanic gillnet M. schmitti in the AUFCZ have been in the Argentine Sea. In Argentina, the fleets operating on the continental shelf. below the total allowable levels and on narrownose smoothhound is mainly Based on CPUE data from these fleets, a decline (CTMFM 2015). However, landed by the commercial fleet the wintering population has likely perhaps the recent decline in M. operating in the Buenos Aires coastal suffered significant declines in schmitti landings prompted the region, and represents up to 14.5 abundance. The CPUE values from both reduction in catch limits in 2015. percent of landings (Carozza et al. 2001 the single and pair trawl fisheries In Brazil, the narrownose cited in Massa et al. 2004b). Between showed an increase from the mid 1970s smoothhound is listed on Annex 1 of 1992 and 1997, landings of the species to the late 1980s; however, after 1987, Brazil’s endangered species list and in Argentina were fairly stable, on the CPUE values for both fleets decreased classified as critically endangered order of 6,000–8,000 t; however, CPUE rapidly, and in 1994, these CPUE values (Directive N° 445). As described in values decreased by upwards of 78 showed an approximate 85 percent previous species assessments, an Annex percent during this time period, abundance decline of M. schmitti from 1 listing prohibits the catch of the indicating a likely decline in the 1985 values (Miranda and Vooren 2003). species except for scientific purposes, abundance of the species. From 1998 to Massa et al. (2006) also cites

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unpublished data that indicate the a higher potential to recover from comprises a single demographic unit in likely extirpation of a local breeding exploitation compared to other coastal the Rı´o de la Plata area and its maritime population of narrownose smoothhound sharks, and could withstand annual front (area separating Uruguay and in Brazil as a result of fishing in inshore removal rates of up to approximately 10 Argentina), with no distinct population pupping and nursery areas. Although no percent of the population. However, structure found between or within the further information was given regarding based on confirmed chronological Rı´o de la Plata, the Atlantic coast or its this population, survey and fisheries reductions in both average size (from outer shelf. These findings indicate high data suggest significant declines in landings data) and total length at connectivity and suggest genetic newborn M. schmitti from a local maturity in the species, it is apparent homogeneity over this geographic range, nursery area off the coast of Rio Grande that removal rates of the species have which is attributed to the likely high do Sul. Once abundant in the 1980s in been exceeding the 10 percent dispersal and migration rates of the the coastal waters off Casino Beach, Rio sustainable removal rate. The reduction species (Pereya et al. 2010). However, a Grande do Sul, neonates of this local in mean size and size at maturity is lack of genetic structure can also result population have since seemingly particularly concerning due to the from many other factors, including large disappeared, with data that show an positive relationship between maternal effective population sizes and/or the absence of individuals from artisanal length and litter size (i.e., litter size presence of shared ancestral beach nets in 2003 and coastal trawl increases significantly with maternal polymorphisms due to recent surveys in 2005 (Vooren et al. 2005b). length) in which a decrease in population divergence. This absence of neonates, compared to maximum size has the potential to In addition to genetic homogeneity, data from the 1980s, is likely a sign of reduce the species’ reproductive output. the study found that nucleotide decline of this population and may even As such, these reductions likely diversity in M. schmitti was lower than suggest a potential extirpation. compromise the species’ growth rate that reported for other elasmobranchs. Overall, best available information and productivity, and consequently, These results may indicate that suggests the species is likely in decline hinder its ability to recover from narrownose smoothhound experienced in parts of its Argentine and Uruguayan exploitation. a genetic bottleneck, recent expansion, range, and has experienced a significant or selection, which potentially occurred decrease in abundance in its winter Spatial Structure/Connectivity during the Pleistocene Era (Pereyra et al. migrant population in Brazil. Although Very limited information is available 2010). However, it is difficult to present abundance estimates are regarding spatial structure and unambiguously discern between unknown, the significant declines in connectivity of M. schmitti populations. evidence for natural selection and both CPUE and landings of the species Tagging studies of related species M. demographic population expansion. throughout its range, as well as the antarcticus and M. lenticulatis found Overall, the low genetic diversity values chronological reduction of the species’ that they have high dispersal capacities found for the species and evidence that average size (based on landings data) (Francis 1988), but no such studies have fishing pressure may have already and size of maturity, suggest been conducted specifically for M. altered the genetic characteristics of the overexploitation of the species and a schmitti. If narrownose smoothhound population (i.e., smaller average size declining abundance trend. Targeting of populations are connected, then the and size at maturity, which in turn can the species will continue, given its significant fishing pressure on the alter reproductive fitness and fecundity) demand in the market and importance migratory population while they winter raise considerable concern over the in both the artisanal and commercial on the Plataforma Sul may be negatively species’ status. This information fisheries in the region and, combined impacting the populations found in indicates that M. schmtti may be at an with the high fishing pressure in the other parts of the species’ range increased risk of inbreeding depression species’ nursery areas, the species may (perhaps contributing to the observed or random genetic drift, and could continue to experience population declines off Argentina and Uruguay). experience the fixing of recessive declines throughout its range, with However, based on the available data, detrimental genes, reducing the overall abundance levels that will likely there is not enough information to fitness of the species. contribute significantly to its extinction identify critical populations or Threats Assessment risk in the foreseeable future. determine whether the rates of dispersal among populations, metapopulations, or The primary threat to narrownose Growth Rate/Productivity habitat patches are posing a risk of smoothhounds is overutilization in The narrownose smoothhound has an extinction. commercial and artisanal fisheries, with estimated lifespan of 20.8 years and 24.7 the species both targeted and bycaught years for males and females, Diversity throughout its range. In Argentina, M. respectively, with a maximum recorded The loss of diversity can increase a schmitti is considered the most size of 110 cm TL. Information species’ extinction risk through important elasmobranch for Argentine regarding size and age of maturity decreasing a species’ capability of fisheries; however, data suggest that the estimates vary throughout the species’ responding to episodic or changing majority of narrownose smoothhounds range, but the most recent estimate from environmental conditions. This can caught by Argentine fishermen are Hozbor et al. (2010) suggests an age at occur through a significant change or juveniles (e.g. up to 81.7 percent of the maturity of 4 years for both sexes. loss of variation in life history landings in 2002), indicating significant Although M. schmitti has an annual characteristics (such as reproductive fishing pressure in important nursery reproductive cycle with a lengthy fitness and fecundity), morphology, areas. Declines in both CPUE and gestation period (11 months) and an behavior, or other genetic biomass of M. schmitti in Argentina average of only 4–5 pups per litter, the characteristics. In terms of population occurred throughout the 1990s and early species’ intrinsic rate of population structure, only one genetics study has 2000s; however, mean values of CPUE increase is relatively high, at 0.175 per been conducted to determine if multiple have shown a slight upward trend from year. Natural mortality rates ranged stocks occur throughout the species’ 2003–2007. However, as noted from 0.139 to 0.412 (Corte´s 2007). These range (Pereya et al. 2010). Results of this previously, these values should be estimates indicate that M. schmitti has study indicate that M. schmitti interpreted with caution as they could

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be the result of increased directed a small population of Brazilian migrants McCormack et al. (2007) note that fishing pressure on M. schmitti or an that was known to give birth in south quotas and size regulations are largely increase in overlap of fishing vessels in Brazil in November and remain through ignored and lack enforcement in areas where M. schmitti has higher February (Massa et al. 2006). Since Argentina. Additionally, since 2006, the concentrations. Further, the 2004, the species has been listed on total number of vessels in Argentina’s chronological reduction in mean size Brazil’s endangered species list, which fishing fleet has remained fairly stable and size of sexual maturity since the prohibits fishers from catching this (OECD 2014), potentially indicating that 1970s indicates overfishing of the species. The species is also listed as one fishing effort has not decreased species, suggesting exploitation rates are of 12 species of concern under Brazil’s substantially in recent years. As such, higher than what the species can FAO NPOA-sharks, which calls for the decreasing landings, even below presently sustain. fishing closures in areas of <20 m deep total allowable catch limits, may In the AUCFZ, where M. schmitti is that would provide protection to indicate a continued decline in the most heavily exploited, fishing neonates and juveniles, as well as other abundance of the species. Overall, based regulations currently set total closures to protect adult aggregations; on the best available information, we permissible catch of M. schmitti at 3,500 however, the implementation and find that existing regulatory measures t (which is a reduction from the 4,500 effectiveness of the recommendations throughout the most heavily exploited t limit that was in place since 2012). outlined in the plan remain uncertain, areas of the species’ range are Additionally, trawling is banned within with the best available information inadequate to protect the species from 5 nm of the coast, which coincides with indicating that current regulatory overutilization, which is the main threat the pupping and breeding areas of the measures in Brazil to protect vulnerable significantly contributing to the species. While there is no information to species are poorly enforced, particularly extinction risk of M. schmitti. indicate whether these regulatory in artisanal fisheries. mechanisms are positively affecting the Risk of Extinction Based on the best available status of the narrownose smoothhound, While there is considerable information, it is evident that M. particularly since species-specific catch uncertainty regarding the species’ schmitti is heavily exploited and has limits for M. schmitti have only been current abundance, the best available likely experienced population declines implemented since 2012, these information indicates that the species throughout its range as a result of regulations may help reduce fishing has experienced population declines of historical and continued overutilization pressure in this important part of the significant magnitude throughout its species’ range. Since 2010, catches of M. of the species. In limited parts of the range. Most concerning is the evidence schmitti in the AUFCZ have been below species’ range, regulatory mechanisms to suggest M. schmitti has undergone a the total allowable levels (for Mustelus are seemingly adequate to control for chronological decline in average size spp. and M. schmitti) and on a decline; overutilization, such as the closures of (based on landings data) and mean size however, it should be noted that despite important nursery areas in Argentina of maturity, as shown in studies from total allowable catch, minimum sizes, which protect neonates and juveniles the 1970s through 2007 (Massa et al. and annual quotas in place for many from fishing mortality. However, 2004a; Corte´s 2007). Not surprisingly, elasmobranchs in Argentina, they are throughout large portions of the species’ this decreasing trend corresponds to an largely ignored and poorly enforced range, particularly in areas where the increase of fishing operations and (McCormack et al. 2007). species is most heavily exploited, it is provides evidence of the negative In Uruguay, narrownose evident that regulatory mechanisms are impact of historical and current smoothhounds are both targeted in not adequately protecting the species exploitation rates and associated fishing artisanal fisheries and caught as from further decline. For example, in mortality on the biological status of the bycatch. Despite the difficulties in the AUCFZ, continued population species. Because of the positive identifying species composition of shark declines have been seen in this part of relationship between maternal length catches and discrepancies in catch the species’ range through 2005 (Massa and litter size for the species, a decrease information, data indicate landings of and Hozbor 2008), despite annual in the average size of the population has M. schmitti have declined in Uruguay, maximum allowable catches for the potential to reduce the species’ and in 2009, the species was classified Mustelus spp. since 2002. Additionally, reproductive output. Furthermore, a as overfished in coastal regions of while CPUE values in Argentina have decrease in average size below the Uruguay and considered a high priority shown a slight upward trend from species’ mean size of maturity can under the country’s FAO NPOA-sharks. 2003–2007, the cause of this trend is hasten the reduction of biomass and In southern Brazil, the intensive uncertain and may actually reflect increase the risk of local extinction fishing effort on the Plataforma Sul has increased direct and indirect fishing (Baum and Myers 2004 cited in Massa likely led to overutilization, and effort on M. schmitti. While species- et al. 2004b). Although the species’ consequently, significant declines in the specific catch limits were implemented relatively high intrinsic rate of winter migrant population of M. for M. schmitti in 2012, it is unclear if population increase and ability to schmitti and potential extirpation of a these levels are adequate to prevent withstand moderate levels of local breeding population. Bottom trawl further declines in the species. exploitation up to 10 percent of the total fishery CPUE data provide evidence that Although corresponding effort data are population provides the narrownose abundance of the winter migrant unavailable, since 2008, landings of M. smoothhound shark with some population of M. schmitti decreased by schmitti reported by Argentina and protection from extinction, and is likely 85 percent due to intensive fishing effort Uruguay to the FAO have decreased by the reason why the species remains the from 1985 onwards. The absence of over 50 percent. Since 2010, catches in most abundant houndshark in the neonates from coastal waters, where the AUFCZ have been below the total Argentine Sea, the aforementioned they were once abundant in the 1980s, allowable catch levels and also on a decreases in average size and size at also suggest that intense fishing effort, decline, which may suggest reducing maturity as well as population size especially in important nursery areas, fishing pressure on the species or suggest the species is being exploited at has led to significant declines in local evidence that catch regulations are a level exceeding what it can sustain. populations and potential extirpation of potentially being followed. However, Thus, based on the best available

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information, we conclude that the species. We therefore propose to list the and the posterior corners are located species is currently at a moderate risk of narrownose smoothhound as a nearer to the origin of the pelvic fin than extinction due to declining trends in threatened species. to the outer corner of the pelvic fins abundance and population growth/ (Vooren and da Silva 1991). The dorsal Angel Sharks productivity, which are unlikely to skin is light to dark brown with several reverse in the foreseeable future because Angel sharks are members of the white or creamy-white to yellowish of the continued overutilization of the family Squatinidae. Both the spiny large, rounded blotches that are variable species in commercial and artisanal angel shark (Squatina guggenheim) and in size and symmetrically distributed on fisheries and inadequacy of existing Argentine angel shark (Squatina the entire dorsal surface (Vaz and regulatory measures to control this level argentina), two of the elasmobranchs Carvalho 2013). of exploitation. considered for listing in this finding, Range and Habitat Use can be found in the Southwestern Protective Efforts Atlantic Ocean from southern Brazil to The spiny angel shark is found in the With the exception of the Argentina. The taxonomy of angel southwestern Atlantic Ocean from recommendations within the FAO sharks of the southwestern Atlantic Espı´rito Santo, Brazil, to Rawson, NPOA-sharks discussed above, we were Ocean has been a source of ongoing Argentina (Milessi et al. 2001; Vo¨gler et unable to find any other information on controversy (Vooren and Chiaramonte al. 2003; Awruch et al. 2008). It is a protective efforts for the conservation of 2006). Due to similar morphological primarily coastal, bottom dwelling angel narrownose smoothhound in Argentina, characteristics, S. argentina, S. shark (Chiaramonte and Vooren 2007; Uruguay, or Brazil that would guggenheim, S. occulta, and S. punctata Crespi-Abril 2013). Spiny angel sharks potentially alter the extinction risk for have been variously synonymized with prefer depths between 10 m and 80 m, the species. We seek additional each other (Compagno 2005; Vooren and but have been reported as deep as 150 information on other conservation Chiaramonte 2006; de Carvalho 2012). m off Argentina (Cousseau 1973; efforts in our public comment process Currently, S. punctata is considered a Chiaramonte and Vooren 2007), and ° (see below). junior synonym of S. guggenheim occur in temperatures between 10 C and 22 °C (Vooren and da Silva 1991). Proposed Determination (Vooren and da Silva 1991; de Carvalho et al. 2012; Vaz and Carvalho 2013). The species lives in muddy or sandy Based on the best available scientific Extensive studies of the morphotypes bottom substrates and is relatively and commercial information as that occur in southern Brazil and the inactive during the day. This nocturnal presented in the status review report southwestern Atlantic concluded that S. activity makes the spiny angel shark and this finding, we find that the argentina, S. guggenheim, and S. more vulnerable to gillnet fisheries, narrownose smoothhound is not occulta are three different species that which tend to operate at night (Vooren presently in danger of extinction can be distinguished by morphological and Klippel 2005a). throughout its range, but likely to differences as well as life history become so in the foreseeable future. We Diet and Feeding characteristics, such as differences in assessed the ESA section 4(a)(1) factors Spiny angel sharks are thought to be reproductive patterns, overall size, and and conclude that the species faces sit-and-wait predators, lying motionless ongoing threats from overutilization and depth and temperature preference on the bottom until prey passes closely inadequacy of existing regulatory (Vooren and da Silva 1991; Vaz and overhead. The prey is then grasped by mechanisms throughout its range. Due Carvalho 2013). An analysis of an upward bite (Vooren and da Silva to the species’ relatively fast population molecular systematics of angel sharks 1991). Based on diet studies, the spiny growth rate (for elasmobranchs) and confirms the validity of S. guggenheim angel shark appears to prefer bony likely high historical abundance, it can and S. occulta as separate species fishes but will also feed on crustaceans, withstand moderate rates of (Stelbrink et al. 2010). molluscs, and polychaetes (Vo¨gler et al. exploitation. However, based on the Spiny Angel Shark (Squatina 2003; Colonello 2005; Vo¨gler et al. declining trends in the species’ guggenheim) 2009). In the AUCFZ, a study of spiny abundance, its low genetic diversity, the angel shark trophic ecology found that, observed decreases in average size of the Species Description numerically, bony fish made up the vast species in catches as well as the The spiny angel shark (S. majority of the diet, at 89.7 percent decreases in size at maturity in areas guggenheim) can be distinguished from (Vo¨gler et al. 2003). Crustaceans (4.8 where it is most heavily exploited, best its sympatric species by the presence of percent), molluscs (4.4 percent), and available data suggest that the fishing a median row of spines or tubercles on polychaetes (0.46 percent) made up the mortality rate is higher than what the its dorsal side (Vooren and da Silva remaining portions (Vo¨gler et al. 2003). species can sustain. Although the 1991; Milessi et al. 2001; Scha¨fer et al. Spiny angel sharks consumed both species’ present level of abundance does 2012; Vaz and Carvalho 2013). There are pelagic and demersal fishes including not appear to be at such a low level to 30–35 spines, which are short, conical, Engraulis anchoita, Cynoscion trigger the onset of depensatory and slightly recurved, between the head guatucupa, Patagonotothen ramsayi, processes, the species’ observed and the first dorsal fin. As females Notothenia longipes, and Merluccius downward trend is unlikely to reverse mature, their dorsal spines become less hubbsi. The crustaceans consumed were in the foreseeable future as a result of distinct and take the form of flattened primarily shrimps (Penaeidae), while continued overutilization. We therefore tubercles, whereas juveniles less than 35 the squid Illex argentinus was the only conclude that the species is on a cm TL of both sexes have spines flanked species of mollusc consumed (Vo¨gler et trajectory indicating that it will more on each side by a diffuse row of smaller al. 2003, 2009). likely than not be at risk of extinction spines (Vooren and da Silva 1991). Although ontogenetic and seasonal in the foreseeable future. We also found Adult males have small spines on the differences in diet have been observed no evidence of protective efforts for the outermost tips of the dorsal surface of for the species (Vo¨gler et al. 2003; conservation of narrownose their pectoral fins that are inclined Colonello 2005; Vo¨gler et al. 2009), smoothhound that would reduce the towards the shark’s midline. The outer bony fish remain the primary prey item level of extinction risk faced by the edges of the pectoral fins are straight for all size classes and during all

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seasons, and, generally, as size of the respectively (Vooren and Klippel Genetics and Population Structure spiny angel shark increases so does its 2005a). Recently, Garcia et al. (2015) In terms of reproduction, the spiny trophic level. Ranging from a minimum examined the population structure of angel shark has only one functional trophic level of 3.69 for the smallest the spiny angel shark in the middle of ovary (Vooren and da Silva 1991), with length group of spiny angel shark (23– its range, in and around the Rio de la the maturation of ovarian follicles 60 cm) to a maximum trophic level of Plata estuary. Using mitochondrial DNA lasting about 2 years before ovulation, 4.40 for the largest length group (81–91 (which is maternally-inherited DNA), followed by gestation (Colonello et al. cm), the entire population of spiny the authors found that individuals from 2007). The female reproductive cycle is angel sharks in the AUFCZ was the outer estuary, surrounding coastal estimated to have a trophic level of 3.90 thought to be triennial (Colonello et al. 2007), with a gestation period that likely sites, and the outer shelf of the (Vo¨gler et al. 2003; 2009). For southwestern Atlantic showed no comparison, in aquatic environments, lasts 12 months (Colonello et al. 2007). Gestation begins in the summer evidence of population genetic trophic levels tend to range from 2 (for structuring. However, examination of species that are lower on the food chain, (January–February) and pupping occurs the following spring (November– nuclear recombinant DNA genes (which such as herbivores and detritivores) to are biparentally-inherited) indicated 5.5 (for predators of marine mammals, December) (Sunye and Vooren 1997). Gestation is divided into two stages: that there was a remarkably high level such as the polar bear and killer whale) of population genetic structure between (Pauly et al. 2014). Uterine gestation and cloacal gestation. Early gestation (January–April) occurs the outer shelf spiny angel sharks and Growth and Reproduction only in the uteri, which contains the coastal and outer estuarine angel sharks. In other words, the samples of Very few age and growth studies on recently ovulated eggs and embryos up to 25 mm TL (Sunye and Vooren 1997). spiny angel shark from the outer shelf the spiny angel shark could be found. In represent an isolated group from the terms of length frequency distributions During mid-term gestation and parturition (June–November) the uteri samples of spiny angel shark from the of spiny angel sharks, individuals coastal and outer estuarine sites. caught in the San Matı´as Gulf, undergo a physical reconfiguration, causing the uteri and cloaca to form a Additionally, mitochondrial DNA Argentina showed a modal peak of 75– indicated that the number of immigrant 90 cm TL for males and 80–95 cm TL heart-shaped chamber where the embryos develop (Sunye and Vooren females per generation from the outer for females, with no evidence of size shelf to the Atlantic coast was much dimorphism (Awruch et al. 2008). The 1997). According to Sunye and Vooren (1997), because this uterine–cloacal lower (2.8 individuals per generation) largest recorded animals were 95 cm TL than the number of immigrant females for both sexes (Awruch et al. 2008). chamber is open to the external environment through a cloacal vent, this per generation between the other Length at 50 percent maturity for males populations (with estimates ranging was reached at 76 cm TL and for anatomical configuration is thought to be the reason why Squatina species are from 12.8–46.9 individuals). All females at 73 cm TL (Awruch et al. analyses revealed very low values of 2008). observed easily aborting embryos during capture or handling. haplotype and nucleotide diversity from Studies of spiny angel sharks farther Pupping occurs during the spring and the recombinant DNA genes. Based on north, in Rio de la Plata and El Rinco´n, summer months (September–March) in the low level of genetic diversity Argentina, found that males from El depths less than 20 m (Vooren 1997; detected in S. guggenheim, Garcia et al. Rinco´n at a given length were Miranda and Vooren 2003). Litter sizes (2015) suggest the species has either significantly heavier than males from for the species range between 2 and 8 undergone a long-term population Rio de la Plata, while females showed pups (Colonello et al. 2007; Vooren and decline or experienced a population no significant differences in the length- Klippel 2005a). For spiny angel sharks bottleneck and recent expansion. Either weight relationship (Colonello et al. in Argentina, Colonello et al. (2007) scenario suggests a vulnerability to 2007). Both sexes grew larger in El estimated an average of 4.07 pups per overexploitation, given the species’ Rinco´n than in Rio de la Plata litter, with fecundity increasing with longevity and low reproductive (Colonello et al. 2007); but, length at 50 female length. In contrast, Vooren and potential. However, additional genetic percent maturity in males was not Klippel (2005a) note that spiny angel studies are needed to better understand significantly different between El sharks in southern Brazil frequently these patterns (Garcia et al. 2015). Rinco´n and Rio de la Plata (75 cm TL have 5 or 6 pups per litter, with the Demography and 72.45 cm TL, respectively). number of pups unrelated to female However, length at 50 percent maturity length. However, given the 3-year Information on natural mortality rates was significantly different between reproductive cycle, the range in pup or the intrinsic rate of population study areas for females, with estimates estimates for spiny angel sharks results increase of the spiny angel shark is of 71.34 cm TL in Rio de la Plata and in a very low annual fecundity for the currently unavailable. 77.01 cm TL in El Rinco´n (Colonello et species (e.g., between 0.67 and 2.67 Historical and Current Distribution and al. 2007). pups per year) (Colonello et al. 2007; Population Abundance In southern Brazil, spiny angel sharks Vooren and Klippel 2005a). After reach a maximum length of 92 cm TL pupping, juveniles of the species will In northern Argentina, spiny angel and age of 12 years (Vooren and Klippel remain in the shallow waters for one sharks are considered to be a 2005a). According to the characteristics year before migrating out to the eurythermic coastal shelf species with for the S. guggenheim population continental shelf (Vooren and da Silva highest abundances on the outer coastal presented in Vooren and Klippel 1991; Vooren 1997; Vooren and Klippel shelf between depths of 28.9 m and 49.6 (2005a), the relative growth rate (k) of 2005a). In terms of known juvenile m (Jaureguizar et al. 2006). In the Rio de the species from the von Bertalanffy habitat, the area of Rio Grande do Sul la Plata estuary, Argentina, spiny angel growth equation is 0.275 year¥1 with a between 31°50′ S. and 33°30′ S. at sharks were present most frequently in theoretical maximum size (L∞) of 94.7 depths less than 20 m is considered a the deepest estuarine zone (12.6 m–16 cm TL. Length and age at first maturity nursery area for spiny angel sharks m) with salinities between 25 and 34 is estimated to be 72 cm TL and 4 years, (Vooren and Klippel 2005a). psu. They are not considered a

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permanent resident of the estuary, with that they were most abundant near 50 m spp. (of which spiny angel sharks are abundances higher in the summer than depths (Rocha et al. 1998). thought to comprise the majority) during the spring and fall (Jaureguizar et In general, very few abundance between the years of 1992 and 1998 al. 2003). estimates are available for the species. (Massa and Hozbor 2003). In the spring In the AUCFZ, spiny angel shark According to Chiaramonte and Vooren of 2003, the estimated biomass of spiny distribution appears to be influenced by (2007), the spiny angel shark is likely angel sharks for all of coastal Argentina temperature, with clear avoidance of composed of smaller, localized was 23,600 t (Massa et al. 2004b). water temperatures below 5 °C and Information about effort was not ° populations throughout its range. In above 20 C (Vo¨gler et al. 2008). Argentinian waters, fishery surveys and provided and more recent abundance or Specifically, Vo¨gler et al. (2008) found commercial data provide limited biomass estimates could not be found. that spiny angel sharks concentrate in In Brazil, there are no biomass ° indication of abundance and trends in water temperatures between 13.2 C and this part of the species’ range. In 1993, estimates for the species and most of the 18.5 °C in the spring and between 7.0 fisheries data for angel sharks is ° ° for example, the abundance of spiny C and 15.0 C in the fall. They prefer angel sharks in the San Matı´as Gulf, grouped into a general Squatina spp. salinities between 33.4 and 33.5, with Argentina (southern Argentina) was category; however, spiny angel sharks avoidance of salinities below 33.0 and estimated to be 192.53 t (Argentina FAO are thought to comprise the majority of above 34.0. Additionally, a strong NPOA-sharks 2009); however, the San the group (Vooren and da Silva 1991; association was found between spiny Matı´as Gulf makes up a very small Cousseau and Figueroa 2001; Vooren angel shark presence and thermal portion (approximately 9.6 percent) of and Klippel 2005a). Off Rio Grande do horizontal fronts, which indicates that Sul (between 35° S. and 28° S.), where the spiny angel shark’s range and no temperature is the principal spiny angel sharks are primarily recent abundance estimates could be environmental variable that influences exploited in Brazil, mean annual found. Surveys of the continental shelf distribution (Vo¨gler et al. 2008). In Rio landings of all angel sharks were over in northern Argentina (between 34° S. de la Plata, in the AUCFZ, spiny angel 2000 t from 1985 to 1994 but fell to 607 and 41° S.; approximately 20 percent of shark densities are particularly high t by 1997. In 1995, mortality rates of S. the species’ range), conducted during along the Uruguayan coast in the spring, guggenheim exceeded population the spring when abundance of spiny which is thought to be related to the growth rates leading to an annual angel sharks is highest, provided presence of higher salinity waters on the population decline rate of 16 percent estimates of mean biomass density of Uruguayan coast than the Argentine (Vooren and Klippel 2005a citing Vieira 0.518 t/nm2 in 1981, 1.305 t/nm2 in coast during this season (Colonello et al. 2 1996). Based on CPUE data from 2007). 1995, and 0.394 t/nm in 1999 fisheries operating in this area, the In southern Brazil, spiny angel sharks (Jaureguizar et al. 2006). Catch rates of population of S. guggenheim is are considered a resident species the species were also fairly high based estimated to have declined by 85 (Vooren 1997). From 1980–1984 spiny on data from trawl research surveys percent between 1986 and 2002 (Vooren angel sharks were common year round conducted in this same area from and Klippel 2005a). Catches of angel on the southern shelf (at depths between October 1997 to June 1998, especially sharks have continued to decline; 10 m and 100 m) from Solida˜o to Chuı´, during the inshore spring/summer however, landings of both S. with some areas recording CPUE migration months (September to March). guggenheim and S. occulta have been densities as high as 50 kg/h (Vooren and Specifically, CPUE ranged from 25 prohibited in Brazil since 2004, and this Klippel 2005a). According to Vooren sharks/30 min of trawling in March to could explain why catches have and Klippel (2005a), a portion of the S. 80 sharks/30 min of trawling in October declined. guggenheim population makes seasonal (Vogler et al. 2008). A later study, migrations across the continental shelf, conducted from 2000–2003 and in the Summary of Factors Affecting the Spiny which is related to the 3-year same area, also recorded high densities Angel Shark reproductive cycle of the species (i.e., of the species during the spring months We reviewed the best available one third of adult females in the (November–December) with estimates of information regarding historical, population will migrate per year to give 750 to <1500 kg/km2 (equivalent to current, and potential threats to the birth). Specifically, this inshore 2.58–5.15 t/nm2) (Colonello et al. 2007). spiny angel shark. We find that the main migration is into depths between 10 m However, based on fishery-independent threat to this species is overutilization and 40 m and occurs in the spring and data collected during research surveys for commercial purposes. We consider summer (September–March) for conducted in the winter of 1993 and the severity of this threat to be pupping and likely mating purposes (as 2004, and spring of 1994, 1999, 2003, somewhat reduced by the species’ adults of both sexes conduct this and 2005, Massa and Hozbor (2008) relatively high abundance in the migration in addition to pregnant observed a decrease in the biomass of S. southern portions of its range; however, females) (Vooren 1997; Miranda and guggenheim, mainly between the winter its demographic characteristics Vooren 2003). As mentioned previously, seasons of 1993 and 2004. Trends in (including very low productivity, newborns remain in these shallow biomass for the spring time cruises were limited connectivity, and low genetic waters (<20 m) for the first year of their less clear, with decreases estimated diversity) increase the susceptibility of life before migrating to deeper waters on between 1994 and 1999 and between the species to depletion and, with the the continental shelf. The other, larger 2003 and 2005, and increases between continued fishing pressure on the portion of the population, which is not 1999 and 2003 (Massa and Hozbor species, places it at an increased risk of moving seasonally and includes both 2008). Declines were also observed in extinction. We summarize information juveniles and adults of both sexes, are the CPUE of fishing fleets operating on regarding these threats and their most abundant in depths of 40 m to 60 the Argentinian shelf, particularly for interactions below according to the m year-round (Vooren and Klippel the smaller-sized vessels (<28 m) that factors specified in section 4(a)(1) of the 2005a). In fact, research surveys off of fish in shallower waters on the shelf and ESA. Available information does not Ubatuba, Sa˜o Paulo, Brazil caught spiny would most likely interact with spiny indicate that habitat destruction or angel sharks in shallow sampling angel sharks. These vessels saw declines curtailment, disease, predation or other stations around 20 m deep, but found of up to 58 percent in CPUE of Squatina natural or manmade factors are

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

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in the mid-1970s, this started to change Klippel (2005a) estimate that the S. al. 2005). The removal of primarily by the early 1980s. For example, in the guggenheim population on the juveniles from a population can have simple trawl fleet, which operated out Plataforma Sul decreased by around 85 significant negative impacts on of Rio Grande in depths of 50 m–100 m percent between 1986 and 2002, with recruitment, especially for a species and engaged in multi-species fisheries the decline occurring simultaneously with a 3-year reproductive cycle. And, directed towards bony fishes (Klippel et with the increase in fishing effort and in fact, in a 2005 bottom trawl survey al. 2005; Vooren and Klippel 2005a), the caused by overexploitation of the conducted in the coastal waters of the proportion of angel sharks (S. species. Plataforma Sul between Torres and guggenheim and S. occulata) in the However, spiny angel sharks are not Chuı´, only neonate spiny angel sharks landings steadily rose from 1975 to only at risk of fishing mortality from the were caught, despite the fact that both 1986. From 1975–1979, the proportion industrial trawl fleets operating on the juveniles and adults would be expected of angel sharks in the landings data was Plataforma Sul, but also from the within the trawled depth range (7 m–20 estimated to be 3.5 percent (range: 2.6– commercial oceanic gillnet fisheries m) (Vooren et al. 2005b). The CPUE of 4.1 percent) and for the period covering which began expanding in the 1990s. As S. guggenheim was also low compared 1980–1986, this had increased to 6.2 the trawl fleets saw catches start to to historical estimates, with an estimate percent (range: 5.3–7.2 percent) (Vooren decline, due to the overexploitation of of only 0.18 kg/h (Vooren et al. 2005b). and Klippel 2005a). Although the the marine resources, many trawlers Despite the decreases observed in simple trawl fleet did not specifically began converting their boats to gillnet spiny angel shark abundance on the target Squatina spp., the increase of vessels in the early 1990s. These vessels Plataforma Sul, fishing effort remains would fish at depths of up to 300 m, high. Additionally, all life stages of angel sharks in landings suggests a with the oceanic bottom gillnet spiny angel sharks are susceptible to the greater interest in the species and fishermen specifically targeting sharks industrial shelf fisheries as the fleets indicates that it was incidentally caught and, based on CPUE data, potentially operate year round covering the entire and retained during regular fishing Squatina species (Miranda and Vooren depth distribution of the species. In fact, operations (Vooren and Klippel 2005a). 2003). The number of gillnet vessels as in 2002, it was estimated that the fishing In 1987, the proportion of angel sharks well as fishing effort increased effort of the industrial trawl fleet from in the landings reached a peak of 9.5 throughout the 1990s, with annual Rio Grande do Sul and Santa Catarina percent, which Vooren and Klippel landings of angel sharks by the oceanic (the two largest fishing fleets operating (2005a) suggest may be evidence of a gillnet fleet of more than 800 t between on the Plataforma Sul) trawled around directed fishery for the species in the the years 1992 to 1998 (Klippel et al. 141,000 km2, corresponding to simple trawl fleet. However, after 1987, 2005). Mazzoleni and Schwingel (1999; approximately 50 percent of the land the angel shark proportion in the cited by Klippel et al. 2005) report that area of the state of Rio Grande do Sul landings significantly decreased, landings of the three angel shark species (Klippel et al. 2005). Hypothetically, if dropping to 5.4 percent in 1990 and 0.5 (S. guggenheim, S. occulta and S. the area swept by each trawl vessel was percent by 2001 (Vooren and Klippel argentina) were common in the Santa different, the 100,907 km2 of the 2005a). The CPUE of angel sharks (S. Catarina bottom gillnet fleet operating Plataforma Sul would be completely guggenheim and S. occulata) by the on the Plataforma Sul between 1994 and swept every 9 months (Klippel et al. simple trawl fleets also decreased over 1999. However, from 1999 to 2002, 2005). When considering the number of this time period, from an average of 2.75 annual landings of angel sharks had gillnet vessels, nets, and the total length t/trip (range: 2.59–3.02 t/trip) from dropped in half (Klippel et al. 2005). of these nets operating on the 1980–1988 to 0.41 t/trip (range: 0.26– The CPUE of the fleet also decreased, Plataforma Sul, it was estimated that the 0.62 t/trip) over the years 1997–2002. from a maximum of 4.3 t/trip in 1992 to length of these gillnets (combined) This 85 percent decrease in CPUE of the values that varied between 0.5 t/trip and would equate to around 8,250 km, species suggests that the declining trend 1 t/trip in the following years (from which corresponds to approximately the in the landings data was likely 1994–2002; Klippel et al. 2005). entire length of the Brazilian coast indicative of overexploitation that led to Likely contributing to the decreases in (Klippel et al. 2005). In 2002, a total of a decline in the species’ abundance in CPUE seen in both the industrial trawl 892 t of angel sharks were landed, with the fishing area where these fleets and gillnet fleets is the fact that the 62 percent landed in Santa Catarina and operate (Vooren and Klippel 2005a). majority of landings from these fisheries 38 percent in the Rio Grande do Sul. Additionally, given that CPUE of angel consist of juvenile angel sharks which, The oceanic gillnet fleet was responsible sharks (S. guggenheim and S. occulata) after spending their first year in depths for most of the landings (42 percent), in the Rio Grande pair trawl fleet also <20 m, migrate out over the continental followed by double-rig trawl fleet (25 declined over this time period, the shelf (see Historical and Current percent), and the coastal gillnet, pair, decrease in abundance of angel sharks Distribution and Population Abundance and single trawl fleets, which each was likely widespread over the section). In an examination of landings contributed about 10 percent of the continental shelf. In the pair trawl fleet, at the Port of Rio Grande between June landings (Klippel et al. 2005). These CPUE decreased from 0.94 t/trip (range: 2002 and July 2003, Klippel et al. (2005) fleets, which historically contributed to 0.34–1.39 t/trip) to 0.12 t/trip (range: found that around 70–85 percent of the the decline in S. guggenheim on the 0.08–0.17 t/trip) between the periods of spiny angel sharks were juveniles (TL Plataforma Sul, remain active today. 1980–1988 and 1997–2002, a decline of <72 cm). The proportion of juveniles Furthermore, as previously discussed 87 percent (Vooren and Klippel 2005a). was highest in the landings from the in the other species assessments, these In 1995, it was estimated that the fishing double-rig trawl fleet, which is to be fleets operate at high efforts on the mortality rate of S. guggenheim had expected as the fleet primarily operates Plataforma Sul and especially within exceeded its population growth rate, in depths <50 m (Klippel et al. 2005). important coastal nursery and inner resulting in an annual rate of population However, the proportion of juveniles shelf habitats for the species. Although decline of 16 percent (Vooren and was still high, around 70 percent, in the landings of the species are currently Klippel 2005a citing Vieira 1996). Based landings of the bottom gillnet, pair, and prohibited, the fleets’ extensive on the above data, as well as data from single trawl fleets, which operate from operations will continue to contribute to fishery research surveys, Vooren and the coast to depths >200 m (Klippel et the fishing mortality of all life stages of

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the species as the spiny angel shark 2007; Massa and Hozbor 2008; Vogler et hubbsi) (Pereyra et al. 2008). Although likely has high discard mortality rates al. 2008), spiny angel sharks are the depth distribution of the spiny angel based on rates estimated for similar commercially exploited. Similar to the shark in Uruguayan waters is angel shark species. For example, the at- narrownose smoothhound, the CTMFM unresolved, in southern Brazilian vessel mortality rate reported for the manages this exploitation through the waters, the species was previously African angelshark (S. africana) is 60 implementation of catch limits and common year-round at depths between percent in prawn trawlers (Fennessy fishery closures. As stated previously, 10 m and 100 m. Specifically, adults 1994) and 67 percent in protective shark the CTMFM implements an annual were frequently found in waters gillnets (Shelmerdine and Cliff 2006). prohibition against demersal trawling in between 40 m and 100 m during the For the Australian angel shark (S. a large section of the AUCFZ, extending autumn and winter and between 10 m australis), mortality rate estimates of 25 across the continental shelf, in order to and 40 m in the spring and summer; and percent and 34 percent have been protect vulnerable chondrichthyans both adults and juveniles were reported for sharks caught in gillnets from fishery-related mortality. The abundant in depths of 40 m–60 m year- (Reid and Krogh 1992; Braccini et al. CTMFM also establishes additional area round (Vooren 1997; Miranda and 2012). These two angel shark species closures to trawling gear throughout the Vooren 2003; Vooren and Klippel have similar life history traits and year in the AUCFZ to protect other 2005a). In northern Argentina, spiny ecology, including: Reproductive species, with these closures also angel sharks displayed highest characteristics (ovoviviparous and indirectly protecting spiny angel sharks abundances on the outer coastal shelf produce small litters; Compagno 1984; from further fishery-related mortality between 29 m and 50 m depths Rowling et al. 2010), maturity and from trawl gear. In terms of the direct (Jaureguizar et al. 2006). Using the maximum sizes (Compagno 1984), management of spiny angel sharks, above depth distribution in areas just depth distribution (continental shelf since 2012, the CTMFM has set a total north and south of Uruguay as a proxy and upper slope), behavior, and diet permissible catch limit for all Squatina for the species’ depth distribution in (mainly teleosts; Shelmerddine and Cliff spp. at 2,600 t (Res. N° 8/14, Res. N° 10/ Uruguayan waters, it is likely that the 2006; Rowling et al. 2010). Given the 13, Res. N° 10/12). In November 2012, proposed fishery closures and trawling general similarities, it seems reasonable this limit was met and landings of bans will provide some level of to infer similar discard survival rates for Squatina spp. were banned for the protection from fishery-related the spiny angel shark from these other month of December (Res. N° 13/12). In mortality, especially during the species’ two Squatina species. As such, given 2013, an additional reserve of 400 t was spring/summer migration to shallower the sensitive life history traits of the proposed to be allowed if the 2,600 t waters for pupping and potentially spiny angel shark as well as the limit was reached; however, total mating purposes. evidence of significant population landings had decreased from the The spiny angel shark is also listed as declines, an assumed 60 percent at- previous year to 2,103 t (CTMFM 2015). a species of high priority in Uruguay’s vessel mortality rate in trawl fisheries In 2014 a 10 percent increase in total FAO NPOA-sharks (Domingo et al. and 25–67 percent mortality in gillnets allowable catch was allowed to be 2008). The plan, as stated previously, is likely to significantly contribute to added to the limit if the CTMFM saw fit has set goals to collect the necessary the overutilization of the species and (Res. N° 10/13, Res. N° 8/14); but this information on its priority species in increase its extinction risk. was unnecessary as landings amounted order to conduct abundance assessments, review current fishing These industrial trawl and gillnet to only 2,281 t (CTMFM 2015). In 2015, fleets currently participate in nationally licenses, and promote public awareness the CTMFM kept the same limit that important fisheries and, as such, the to release captured individuals. was implemented in 2014 (2,600 t with threat they pose to S. guggenheim is However, no updated results from the an allowance of 10 percent increase; unlikely to decrease in the foreseeable goals and priorities of this plan could be Res. N° 07/15). Although McCormack et future. In fact, in the oceanic drift found. al. (2007) report that elasmobranch gillnet fishery, the fishery responsible In Brazil, the spiny angel shark is quotas and size regulations are largely for the highest landings of angel sharks, listed on Annex 1 of Brazil’s endangered ignored in Argentina and poorly the main fish species targeted (Umbrina species list and classified as critically enforced, Squatina landings have been canosai, Cynoscion guatucupa, and endangered (Directive N° 445). As below the maximum catch limit in Micropogonias furnieri) represented described in previous species accounts, around 12.8 percent of the total national recent years, providing evidence that an Annex 1 listing prohibits the catch of marine fish landings in 2011 for all of regulations are potentially being the species except for scientific Brazil. Micropogonias furnieri is the followed. However, without effort purposes, which requires a special second most landed fish nationally, and information, it is unclear whether these license from IBAMA. There is also a U. canosai is the seventh most landed. regulations and the corresponding prohibition of trawl fishing within three Based on the above information, the decreases in landings can be attributed nautical miles from the coast of significant level of fishing effort and to adequate control of the exploitation southern Brazil, although the associated fishing mortality, especially of the species or rather reflects the lower enforcement of this prohibition has been of juvenile angel sharks, likely caused abundance of the species from declining noted as difficult (Chiaramonte and and will continue to cause substantial populations, or more likely a Vooren 2007). In addition, the species is declines in the spiny angel shark combination of the two scenarios. still susceptible to being caught as population. In Uruguay, regulations that likely bycatch in the legally permitted coastal contribute to decreasing the fishery- gillnet fisheries and offshore trawl and Inadequacy of Existing Regulatory related mortality of the species include gillnet fisheries and vulnerable to the Mechanisms a summer trawling ban in 25 m to 50 m associated bycatch mortality (Lessa and In the AUCFZ, the area comprising depths between La Paloma and Chuy Vooren 2007). The spiny angelshark is around one quarter of the species’ range, and specific fishery area closures in the also listed as one of the 12 species of and where survey data suggest the spring, summer, and autumn on the concern under Brazil’s FAO NPOA- species is likely at highest concentration Uruguayan continental shelf, designated sharks and would benefit from the (Jaureguizar et al. 2006; Colonello et al. to protect juvenile hake (Merluccius proposed fishing closures and other

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management measures outlined in the Sul in both the single and pair trawl spiny angel shark likely led to the plan. This includes the fishing fishing fleets over the time periods of species being the most common angel moratorium and marketing ban, which 1980–1988 and 1997–2002, the shark found in the southwest Atlantic. is proposed to be in effect until there is population of S. guggenheim off However, despite its fast growth rates, scientific evidence that supports southern Brazil has declined by around the spiny angel shark has a significantly population recovery of the spiny angel 85 percent since 1985 (Miranda and lengthy reproductive cycle of 3 years, shark. It also suggests that a fishing Vooren 2003; Vooren and Klippel with a litter size ranging between 2 and exclusion area be established in the 2005a). More recent landings data from 8 pups and an average of around 4–5 coastal zone (specifically over a large the Santa Catarina oceanic gillnet pups/litter. This translates to an annual region of the coast of Rio Grande do Sul fishery, covering the years 2001–2010, fecundity between 0.67 and 2.67 pups at depths of 20 m) to protect important show a peak in angel shark landings in per year. Spiny angel sharks are also nursery grounds for the species. 2004 of 340 mt before significantly thought to have cloacal gestation during However, as mentioned previously, the dropping, with only 2.6 mt landed in the latter half of pregnancy, which is plan was only just approved as of 2010. However, in 2004, landings of S. thought to be the reason why Squatina December 2014 and will not be fully guggenheim along with S. occulta were species are observed easily aborting implemented for another 5 years. Thus, prohibited and, as such, the decline in embryos during capture or handling. the implementation and effectiveness of landings data after 2004 may be a Given the already low annual fecundity the recommendations outlined in the reflection of this prohibition. of the species, any further loss of plan remain uncertain, with the best Based on the commercial fishery embryos would significantly decrease available information indicating that information, it is likely that spiny angel their already low reproductive output. current regulatory measures in Brazil to sharks have experienced varying levels Overall, these reproductive protect vulnerable species are poorly of population decline throughout its characteristics suggest the species has enforced. range. In the northern half of the relatively low productivity, similar to species’ range (off Brazil), the best other elasmobranch species, which may Extinction Risk available information indicates the hinder the species’ ability to quickly The best available information species has undergone rather substantial rebound from threats that decrease its provides multiple lines of evidence population declines, with evidence of abundance (such as overutilization) and indicating that the S. guggenheim negative population growth rates that render the spiny angel shark more currently faces a moderate risk of led to significant decreases in the vulnerable to extinction in the face of extinction. Below, we present the overall abundance of the species to the other demographic risks and threats. point where catch rates and demographic risk analysis, threats Spatial Structure/Connectivity assessment, and the overall risk of observations of spiny angel sharks are extinction for the spiny angel shark. extremely low. Off Uruguay and The spiny angel shark has a Argentina, where reported biomass widespread range in the southwest Demographic Risk Analysis estimates suggest the species was and is Atlantic but is thought to be comprised Abundance likely still most concentrated, the higher of smaller, more localized populations abundance levels may explain why the (Chiaramonte and Vooren 2007); Spiny angel sharks are likely the most magnitude of population decline is however, information to support this is abundant angel shark species from estimated to be smaller in this portion currently unavailable. Information on southern Brazil to Argentina; however, of the species’ range. Therefore, while the connectivity among S. guggenheim current quantitative estimates of the species may not be of such low populations throughout its range is abundance of the species throughout its abundance such that it is currently at limited. The populations occurring on range are unavailable. In Argentina, the risk of extinction, given the high the Plataforma Sul, off southern Brazil, abundance of spiny angel sharks in the exploitation of the species throughout are assumed to carry out their entire San Matı´as Gulf (which comprises its range and subsequent population lifecycle within the same area. This around 9.6 percent of the species’ range) decline in the northern half, coupled behavior indicates that these was estimated to be 192.53 t in 1993. In with the species’ low productivity, populations maintain population 2003, the estimated biomass of spiny abundance levels will likely continue to growth by recruiting within each area angel sharks for all of coastal Argentina decline through the foreseeable future to without producing a necessary excess of was 23,600 t. No other population the point where it may be a significant recruits with the potential to migrate to estimates have been calculated for the contributing factor to the species’ other areas (Vooren and Klippel 2005a). species. Additionally, between 1981 and overall extinction risk. As a result, S. guggenheim populations 2004, catch rates and density estimates on the Plataforma Sul likely have for areas off the Argentine continental Growth Rate/Productivity limited movement and dispersal shelf have been variable; however, There is minimal information on the migration between neighboring fishing fleets reported declines of up to growth rate and productivity of the populations, with migrants having no 58 percent in CPUE between 1992 and species. Based on the estimated von impact on the short term abundance of 1998. Bertalanffy growth parameters, the a population. Based on genetic studies, In Brazil, quantitative information, in spiny angel shark exhibits rather fast there is also evidence of limited the form of CPUE and landings data for growth rates for a shark species (with a connectivity between populations found the fishing fleets operating on the growth coefficient (k) of 0.275/year; in other parts of the species’ range. For Plataforma Sul, is available for all angel Vooren and Klippel 2005a). Fast growth example, genetic analyses of individuals shark species, of which S. guggenheim rates help protect species from found around the Rio de la Plata estuary likely comprises a majority. These data extinction by allowing species to attain indicate a high level of population provide insight into trends in larger sizes at earlier ages, protecting it genetic structure between the spiny abundance of the spiny angel shark in from predation, and also allowing angel sharks that occur on the outer roughly 20 percent of its range. Based species to attain sexual maturity sooner, shelf and those that are found in the on a comparison of the CPUE estimates thereby contributing to population outer estuarine and coastal waters (with of angel sharks caught on the Plataforma growth. The fast growth rates of the very few immigrants between these

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populations) (Garcia et al. 2015). In population saw declines of up to 58 mortality rates exceeding population other words, the evidence of limited percent in the late 1990s. Although growth rates and resulting in an annual inter-population exchange observed in exploitation of the species in the rate of population decline of 16 percent the species reduces the recovery AUCFZ, where the species appears to be for spiny angel sharks in the mid 1990s potential for the depleted and small at highest concentration, has been (Vorren and Klippel 2005a). Although local populations found throughout the managed since 2012 with area closures many trawlers began converting their range, and may increase the risk of local and catch limits, the lack of recent boats to gillnet vessels in the early extirpations, possibly leading to abundance estimates or trends hinders 1990s (due to decreases in catch), the complete extinction. an evaluation of the adequacy of current threat of overutilization remains as the regulatory measures in preventing the oceanic bottom gillnet fishermen also Diversity overutilization of the species from this fish at depths of up to 300 m and now A recent genetic analysis using portion of its range. It is important to land the majority of angel sharks, of maternally-inherited mitochondrial note that landings prior to 2012 from which 70–85 percent are juveniles DNA markers from spiny angel sharks in this area were on the same order of (Klippel et al. 2005). Although spiny and around the Rio de la Plata Estuary magnitude as those reported for all of angel sharks have been a prohibited (approximately mid point of the species’ Argentina and which subsequently led species since 2004, the fishing effort range) found no evidence of population to the declines observed in the late (both by trawl and gillnet fleets) on the genetic structuring (Garcia et al. 2015). 1990s. Landings have since decreased Plataforma Sul remains high and poorly However, analyses using biparentally- since the implementation of the catch regulated, and, therefore, the inherited nuclear recombinant DNA limits, and appear to be on a declining susceptibility of the species’ to fishery- genes indicated that there was a trend; however, the number of fishing related mortality also remains high. The remarkably high level of population vessels authorized to operate in the industrial gillnet and trawl fleets, which genetic structure between spiny angel AUCFZ has remained fairly stable, contributed to the historical decline in sharks found on outer shelf and those in potentially indicating that fishing effort the population off southern Brazil, are the coastal and outer estuarine areas has not decreased substantially in recent active today and participate in (Garcia et al. 2015). The combination of years. In other words, the recent nationally important fisheries. Given the low haplotype and high nucleotide declining trend in landings, even below percentage of juveniles caught by these diversity can be indicative of a transient total allowable catch limits, may fisheries coupled with the assumed bottleneck in the ancestral population, indicate decreasing abundance of the discard mortality rates, the continued or an admixture of samples from small, species in this part of its range. operations of these fleets will likely geographically subdivided populations, In Uruguay, spiny angel sharks are have significant negative impacts on S. with the genetic patterns of exchange both targeted and caught as bycatch by guggenheim recruitment to the potentially explained by sex-biased industrial trawling fleets in coastal and population, especially for a species with behavior or long term shifts in spatial offshore waters (Vo¨gler et al. 2008; a 3-year reproductive cycle. The present and temporal environmental variables Domingo et al. 2008). All life stages of level of fishing effort by the artisanal leading to current displacements (Garcia the species are exploited as the fleets and industrial fisheries on Brazil’s et al. 2015). However, overall, the low operate over the entire depth range of continental shelf will continue to lead levels of genetic diversity in spiny angel the species (between 10 m and 200 m). to declines in the spiny angel shark shark populations suggest a Abundance and trends of the species population and, hence, contribute to the vulnerability to overexploitation in the within this region are unknown; extinction risk of the species. southwestern Atlantic Ocean (Garcia et however, declines in populations just al. 2015) and will likely render the north and south of this region have been Risk of Extinction spiny angel shark more susceptible to observed, with the species listed as high There is significant uncertainty extinction in the face of other priority in Uruguay’s FAO NPOA- regarding the current abundance of the demographic risks and threats. sharks. Additionally, landings of angel species throughout its entire range. sharks by Uruguayan vessels in the While the Brazilian populations have Threats Assessment AUCFZ have increased in both number experienced substantial declines and The primary threat to S. guggenheim and proportion of total angel shark remain at risk from overutilization by is overutilization in artisanal and landings in the AUCFZ, indicating a fisheries, the same cannot be concluded commercial fisheries. The vast majority potential increase in fishing effort of with certainty for the populations of fisheries information on angel sharks this vulnerable species. farther south in the species’ range. is generally reported as ‘‘Squatina spp’’ In Brazil, spiny angel sharks have Based on the available data, the throughout Brazil, Uruguay, and been heavily exploited by industrial populations off Uruguay and Argentina Argentina; however, spiny angel sharks trawlers and gillnet fleets since the have likely experienced moderate are thought to be the most abundant 1980s (Haimovici 1998; Vo¨gler et al. declines, with recent landings and angel shark species from southern Brazil 2008). In southern Brazil, angel shark vessel data potentially indicating a to Argentina and, therefore, likely landings are recorded in industrial decreasing trend in abundance and comprise the majority of the Squatina single trawl, pair trawl, oceanic bottom stable or increasing trend in fishing species that are landed. gillnet, and coastal artisanal fisheries. effort. The significant demographic risks In Argentina, although the species is These industrial and coastal artisanal to the species (e.g., extremely low not directly targeted, they are caught fleets operate year round in depths that fecundity, declining population growth incidentally in multispecies artisanal span <20 m to 300 m, including during rate, and limited connectivity), the shark fisheries and are considered a the sharks’ reproductive seasonal decline and subsequent rarity of the valuable bycatch species (Chiaramonte migrations, and hence capture all life species in an area that comprises around 1998; Bornatowski et al. 2011). Fishery- stages of spiny angel sharks (Vooren and half of its range, and the evidence of independent research surveys have Klippel 2005a). The impact of this continued and heavy fishing pressure recorded relatively high densities of the fishing pressure and effort led to on the species throughout its entire species on the Argentinian shelf; observed declines in S. guggenheim range, place the species on a trajectory however, based on CPUE data, the (around 85 percent), with fishing indicating that it will more likely than

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not be at a high level of extinction risk Argentine Angel Shark (Squatina Diet and Feeding in the foreseeable future. Therefore, argentina) Like the spiny angel shark, the based on the best available information Species Description Argentine angel shark is thought to be and the above analysis, we conclude a sit-and-wait predator, lying motionless that S. guggenheim is presently at a In addition to the spiny angel shark, on the bottom until prey passes closely moderate risk of extinction throughout the Argentine angel shark was overhead. The prey is then grasped by its range. petitioned for listing under the ESA. an upward bite (Vooren and da Silva Protective Efforts The Argentine angel shark occurs in the 1991). There is limited information Southwest Atlantic and can be regarding the Argentine angel shark With the exception of the distinguished from its sympatric species diet. In a study that analyzed stomach recommendations within the FAO by its coloration, dental formula, contents of 53 individuals, results NPOA-sharks discussed above, we were neurocranial features, dorsal surface showed that fish made up 68.33 percent unable to find any other information on denticle pattern, and pectoral fin shape. of the diet, and crustaceans and protective efforts for the conservation of Unlike S. guggenheim, the Argentine molluscs made up 15 percent and 1.6 spiny angel sharks in Argentina, angel shark lacks a dorsal midline of percent of the diet, respectively Uruguay, or Brazil that would morphologically distinct denticles (Vaz (Cousseau 1973). The rest of the diet potentially alter the extinction risk for and Carvalho 2013). Dermal denticles contained unidentifiable remains. The the species. We seek additional densely cover the entire dorsal surface, most common fish species was information on other conservation except for the posterior margins of Cynoscion striatus, while the shrimp efforts in our public comment process unpaired fins and the anterior apex of Artemesia longinaris and (see below). the pectoral fins. The pectoral fins are Hymenopenaeus mulleri were the most common crustaceans, and Loligo Proposed Determination large, twice as long as they are wide, with the anterior margins strongly brasiliensis was the most common Based on the best available scientific convex, creating a visible ‘‘shoulder’’ mollusc (Cousseau 1973). Argentine and commercial information as area at the base of the head (Vaz and angel sharks are also thought to presented in the status review report Carvalho 2013). The dorsal coloration is occasionally consume the short-finned squid (Illex argentinus) (dos Santos and and this finding, we find that the spiny dark to purplish brown with small, Haimovici 2000). angel shark is not presently in danger of round, white spots symmetrically extinction throughout its range but distributed across the entire dorsal Growth and Reproduction likely to become so in the foreseeable surface (Vooren and da Silva 1991; Little is known about the growth and future. We assessed the ESA section Milessi et al. 2001; Vaz and Carvalho 4(a)(1) factors and conclude that the reproduction of the Argentine angel 2013). Small individuals are creamy shark. Their maximum total length is species faces ongoing threats from white over the entire ventral surface, overutilization and inadequacy of estimated at 138 cm with a size at while larger animals develop dark beige sexual maturity of 120 cm TL; however, existing regulatory mechanisms on the central region of the head, throughout its range. Due to the species’ age at first maturity and size at birth are margins of the pectoral fins, origin of unknown (Vooren and da Silva 1991; relatively fast growth rate (for the pelvic fins, and the posterior region elasmobranchs) and high biomass in the Vooren and Klippel 2005a). Gravid of the trunk (Vaz and Carvalho 2013). females and neonates are rarely found, southern portion of its range, the species Unlike S. guggenheim and S. occulta, has not yet declined to abundance levels so little is known about the reproductive female Argentine angel sharks have two characteristics of the species. Gestation that would likely trigger the onset of functional ovaries, which can also serve is lecithotrophic (developing embryos depensatory processes. However, the as an identifying feature (Vooren and da depend on yolk for nutrition) (Vooren species’ demographic risks (including Silva 1991). 1997) and litter size ranges from 7–11 very low fecundity, low genetic pups (most commonly 9 or 10 pups) diversity, and connectivity) coupled Range and Habitat Use (Vooren and Klippel 2005a). Like S. with the significant reduction in the occulta and S. guggenheim, the population from the northern portion of While there is some conflicting Argentine angel shark may have cloacal its range, greatly increases the species’ information regarding the range of gestation during the latter half of vulnerability to extinction from Argentine angel shark, it is clear that they have a restricted range in the pregnancy (Vooren and Klippel 2005a). environmental variation or Based on the location and capture of anthropogenic perturbations. Southwest Atlantic, and are present in southern Brazil (from Rio de Janeiro two neonates of 35 cm and 37 cm TL in Furthermore, given the evidence of Santa Catarina, Brazil, it is assumed that decreasing landings despite stable (or southward), Uruguay, and at least the northern part of Argentina (i.e., Buenos Argentine angel sharks reproduce on the even increasing) fishing effort, we find slope of the southern Brazilian Aires). Argentine angel sharks live on that the level of exploitation in the area continental shelf (Vooren and Klippel muddy or sandy bottom substrates on where spiny angel sharks are currently 2005a). Additionally, the Bahia Engano the continental shelf and slope at depths most concentrated is likely contributing in coastal Patagonia is thought to serve between 100 m and 400 m, with a to unsustainable fishing mortality rates. as a nursery area for the Argentine angel principal depth range of 120 m–320 m We therefore conclude that the species shark (Van der Molen et al. 1998). is on a trajectory indicating that it will (Cousseau 1973; Vooren and da Silva more likely than not be at risk of 1991; Vooren and Klippel 2005a). Angel Genetics and Population Structure extinction in the foreseeable future. We sharks are active mostly at night, and Studies examining the genetics of the also found no evidence of protective show limited movement and dispersal species or information on its population efforts for the conservation of spiny migration between neighboring structure could not be found. angel sharks that would reduce the level populations, with migrants having no of extinction risk faced by the species. impact on the short term abundance of Demography We therefore propose to list the spiny a population (Vooren and Klippel Information regarding natural angel shark as a threatened species. 2005a). mortality rates or the intrinsic rate of

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population increase of the Argentine according to the factors specified in total biomass of the population angel shark is currently unknown. section 4(a)(1) of the ESA. Available estimated from the early 1980s, at information does not indicate that 3,974.7 mt, and landings remained near Historical and Current Distribution and habitat destruction or modification, this level in 1994 at 3,621.8 mt Population Abundance disease, predation or other natural or (Chiaramonte 1998). However, by 1998, As previously described, there is manmade factors are operative threats CPUE values indicated that the level of conflicting information regarding the on these species; therefore, we do not fishing mortality on the Squatina shark range of the Argentine angel shark, and discuss these factors further in this populations was leading to declines in the species’ distribution is poorly finding. See Casselbury and Carlson abundance of angel sharks. Specifically, defined. While there are no specific (2015f) for discussion of these ESA Massa and Hozbor (2003) estimated that population abundance estimates for section 4(a)(1) threat categories. CPUE of angel sharks declined by 58 Argentine angel sharks, they are percent between 1992 and 1998 for Overutilization for Commercial, considered to be the least common vessels operating on the Argentine shelf, Recreational, Scientific or Educational species of angel shark found in the and since 1998, landings of Squatina Purposes southwestern Atlantic, particularly in species have been on a decline (Massa Argentina (Vooren and Klippel 2005a). The primary threat to S. argentina is et al. 2004b). According to one paper, Argentine angel overutilization by commercial fisheries, In Uruguay, Argentine angel sharks sharks occur in highest densities (from particularly the trawl and bottom gillnet are targeted in the Atlantic gillnet 1 to 11.4 t/nm2) along the Uruguayan fisheries in Brazil, where the species is fishery and bottom trawl fisheries. They coast in the AUCFZ, where salinities are likely most concentrated. As mentioned are also caught as bycatch in bottom higher than the Argentine coast (Dı´az de previously, the vast majority of fisheries longline, estuarine gillnet, and bottom Astarloa et al. 1997). However, this information on angel sharks is trawl fisheries (Domingo et al. 2008). paper refers to all Squatina species as documented as ‘‘Squatina spp’’ Both artisanal and industrial trawl fleets Argentine angel sharks and, based on throughout Brazil, Uruguay, and operate at depths between 10 m and 200 the distribution of S. guggenheim (see Argentina; however, the Argentine angel m in Uruguay, which overlap with the species assessment; Colonello et al. shark is the rarest Squatina species in principal depth range of S. argentina. 2007), the authors have likely the region. Additionally, incorrect Annual catches of all angel sharks in misidentified spiny angel sharks as species identification of angel sharks is Uruguay have increased over time, with Argentine angel sharks. a problem that persists in the AUCFZ, less than 100 t landed from 1977 to 1996 In Brazil, Argentine angel sharks of all particularly in Argentine landings and increasing to between 200 t and 400 life stages are most abundant between (Milessi et al. 2001); therefore, t from 1997 to 2005. In 2012, catches for Rio Grande and Chuı´ in Rio Grande do determining the magnitude of threats Squatina spp. exceeded the set catch Sul, with no evidence of abundant currently acting specifically on S. limit in the AUCFZ (2,600 t), resulting populations outside of this area (Vooren argentina is challenging. However, some in the closure of the fishery for the and Klippel 2005a; Vooren and information, including fisheries effort, following month. However, similar to Chiaramonte 2006). Specifically, the catch and landings data, provides catch composition reported in outer shelf and upper slope of the insight into the current status of Argentina, it is likely that the majority southern Brazilian continental shelf, Argentine angel shark, as described of these reported angel shark landings south of latitude 32 °S., are important below. are spiny angel sharks rather than habitat areas for S. argentina. However, As discussed in the spiny angel shark Argentine angel sharks (Domingo et al. based on fishery independent research assessment, angel sharks, in general, 2008). surveys from 1986–2002, the have been historically caught in the In Brazil, Argentine angel sharks are abundances of both the Argentine angel multispecies artisanal shark fisheries most abundant between Rio Grande and shark and the hidden angel shark (S. and considered valuable bycatch species Chuı´ in Rio Grande do Sul, off southern occulta) within this area have declined in Argentina (see spiny angel shark: Brazil (Vooren and Klippel 2005a; by approximately 80 percent (Vooren Overutilization section). However, the Vooren and Chiaramonte 2006); and Klippel 2005a). Argentine angel shark is considered however, they are the least captured relatively rare in Argentina (Menni et al. Squatina species in Brazilian fisheries Summary of Factors Affecting the 1984 cited in Vooren and Klippel (Perez and Wahlrich 2005). In general, Argentine Angel Shark 2005a), with S. guggenheim comprising angel shark landings are recorded in We reviewed the best available the majority of the catch (Massa et al. single trawl, pair trawl, oceanic gillnet, information regarding historical, 2004b). From 1981–1982, Otero et al. and coastal artisanal fisheries. current, and potential threats to the (1982) noted the low density of S. Historically, angel sharks were fished on Argentine angel shark species. We find argentina off the Buenos Aires coast and the Brazilian shelf by double rig that the main threat to this species is estimated an annual biomass of only trawlers down to 140 m depths, with S. overutilization for commercial 4,050 t. In the 1990s, angel sharks guggenheim comprising the majority of purposes. We consider the severity of became commercially important the catch (Haimovici 1998). this threat to be exacerbated by the bycatch, particularly in the Necochea As catch rates of shelf resources species’ natural biological vulnerability school shark (Galeorhinus galeus) decreased, and international markets for to overexploitation, which has led to gillnet fishery, and were a prevalent traditionally discarded or poorly known significant declines in abundance of the bycatch species in the Patagonian species expanded, deep-water demersal species. We find current regulatory coastal trawl fisheries. According to fishing operations off southern Brazil measures inadequate to protect the 1993–1996 observer data from the (from 20° S.–34° S.) increased in the species from further overutilization. Patagonian fishery, Argentine angel early 1990s (Valentini et al. 1991; Hence, we identify these factors as sharks were bycaught with medium Haimovici 1998) and greatly accelerated additional threats contributing to the frequency, particularly in the San after 1999. This was largely a result of species’ risk of extinction. We Matias Gulf and Bahia Engano. By 1993, shrimp and groundfish trawlers summarize information regarding these declared landings of S. argentina were expanding their fishing grounds towards threats and their interactions below on the same order of magnitude as the the previously unexploited resources of

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

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mortality rate in trawl fisheries and proposed rule, the Argentine angel EEZ, which were responsible for ∼25–67 percent mortality in gillnets). shark was listed as ‘‘critically catching a total of 157,656 monkfish Thus, while the bottom gillnet fishery endangered’’ under Annex I of Brazil’s (compared to a total of only 16,697 specifically targeting monkfish has been endangered species list in 2004. As monkfish landed by all gears of the restricted in terms of overall effort, with described in previous species national fleet) from 2000–2007, and only the national trawl fleet continuing assessments, an Annex 1 listing recent catch limits of 1,500 tons for the to operate on the upper slope (Perez et prohibits the catch of the species except gillnet fishery, have likely reduced the al. 2009), the threat of overutilization for scientific purposes, which requires a level of fishing pressure and subsequent remains. However, the monkfish fishery special license from IBAMA. There is mortality of Argentine angel sharks. is not the only fishery presently also a prohibition of trawl fishing However, the fact that enforcement of operating within the Argentine angel within three nautical miles from the management rules for the monkfish shark habitat. There are a number of coast of southern Brazil, although fishery has been poor, with no evident oceanic bottom gillnet fisheries targeting enforcement of this prohibition has been signs of recovery for this overexploited other species (e.g., Umbrina canosai, noted as difficult (Chiaramonte and resource (Perez et al. 2009), may Cynoscion guatucupa, and Vooren 2007), and moreover, the ban indicate that the regulations outlined in Micropogonias furnieri) that currently only covers depths of <10 m, which the management plan for the monkfish operate on the shelf and slope at depths does little to provide any protection to are inadequate to control for indirect of up to 300 m. In fact, due to their effort the Argentine angel shark given its overutilization of Argentine angel and fishing area of operation, these principal depth distribution of 120–320 sharks. Given that the conservation oceanic bottom gillnet fisheries now m. As described in previous species status of the Argentine angel shark land the majority of angel sharks in assessments, Brazil has a FAO NPOA- likely relies heavily upon the success of Brazil (Klippel et al. 2005). As described sharks; however, the Argentine angel the management plan for the southern in the spiny angel shark assessment, shark is not considered one of the 12 Brazil gillnet monkfish fishery (Vooren fishing effort (both by trawl and gillnet species of concern. and Chiaramonte 2006) and that the fleets) on the Plataforma Sul remains Finally, there are some regulatory monkfish fishery is still operational high and poorly regulated, and mechanisms in place for the monkfish throughout the species’ Brazilian range therefore, the susceptibility of the fishery in Brazil, which operates in the via the national fleet, with reportedly species’ to fishery-related mortality also primary habitat of the Argentine angel poor enforcement of management rules, remains high. As such, given the best shark and has been a significant source the fishery is likely still exerting fishing available information and the above of bycatch-related mortality for the pressure and contributing to the analysis, we conclude that species. In mid-2002, government overutilization of the already at-risk S. overutilization is a factor that is regulations were implemented to argentina population. This continued significantly contributing to the prohibit foreign gillnetters from exploitation is concerning for a species extinction risk of the species. operating south of 21°S (to the southern that has already undergone such extent of Brazil’s EEZ), which roughly Inadequacy of Existing Regulatory significant declines in a critical portion encompasses the entirety of the Mechanisms of its range, with no indication of a Argentine angel shark’s Brazilian range. reversal of this trend. As such, we In Argentina, catches of angel sharks This regulation effectively terminated conclude that existing regulatory are regulated through annual catch foreign chartered gillnet operations off mechanisms to control for limits and fisheries closures. Since Brazil and left a national fleet of 5 overutilization of the Argentine angel 2013, Squatina landings have been licensed units to continue the fishery shark are inadequate, particularly in below the maximum catch limit in (Perez et al. 2009). However, despite Brazil, where the species is most heavily recent years, providing evidence that this reduction of the monkfish fishery concentrated and utilized. regulations are potentially being fleet, uncontrolled exploitation followed. However, without effort continued and the stock was declared Extinction Risk information, it is unclear whether these overexploited in 2004. It was not until Demographic Risk Analysis regulations are adequately controlling 2005 that a management plan for the the exploitation of angel sharks and monkfish fishery was eventually Abundance given that Argentine angel sharks are developed, which included the Estimates of population abundance particularly rare in Argentina, the implementation of 100 percent observer specifically for Argentine angel shark degree to which these regulations are coverage for monitoring the fishery, (Squatina argentina) throughout its decreasing the threat of overutilization logbooks, and a recommendation to ban range are not available. However, some of the species in this portion of its range fishing shallower than 250 m (Perez et qualitative information as well as is uncertain. al. 2009). However, the principal depth density and biomass estimates are In Uruguay, the Argentine angel shark range of S. argentina exceeds the 250 m available from parts of the species’ is listed as a species of high priority in restriction, thus this recommendation range. Compared to congeners S. the country’s FAO NPOA-sharks only theoretically protects a portion of guggenheim and S. occulta, the (Domingo et al. 2008). The plan, as the species’ depth range. In 2008, catch Argentine angel shark is the rarest stated previously, has set goals to collect limits of 1,500 t per year were imposed species of angel shark found in the the necessary information on its priority for the monkfish gillnet fishery, as well southwestern Atlantic, particularly in species in order to conduct abundance as bycatch limits of certain species; Argentina. Biomass of S. argentina in assessments, review current fishing however, though the catch limits should Argentina was estimated to be 40,000 mt licenses, and promote public awareness help reduce overall fishing effort, the in 1998, although there is high to release captured individuals. species is still susceptible to bycatch- uncertainty with this estimate. In Brazil, However, no updated results from the related mortality in the fishery. this species is reportedly most abundant goals and priorities of this plan could be Overall, regulatory mechanisms for between Rio Grande and Chuı´ in Rio found. the monkfish fishery, particularly the Grande do Sul, with no evidence of Like the spiny angel shark, and other ban of chartered foreign gillnets from abundant populations outside this species described previously in this 21° S. to the southern extent of Brazil’s region. Based on fishery-independent

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surveys conducted from 1986–2002, and assumed to carry out their entire magnitude of threats currently acting abundance of Argentine angel shark lifecycles within the same area. This specifically on S. argentina is declined by approximately 80 percent indicates that populations of the species challenging. However, there are some on the outer shelf and upper slope of the maintain population growth by landings and CPUE data for S. Plataforma Sul, which is where the recruiting within each area without argentina, which suggest the historical highest concentrations of the species is producing a necessary excess of recruits and continued level of fishing pressure located. Due to uncertainties regarding with the potential to migrate to other has led to significant observed declines the range and distribution of the areas (Vooren and Klippel 2005a). As a in the species. species, as well as identification issues result, S. argentina populations Historically, angel sharks, including between S. argentina and other reportedly have limited movement and S. argentina, were caught in Squatina spp. in the region, the current dispersal migration between multispecies artisanal shark fisheries abundance of the species cannot be neighboring populations, with migrants and considered a valuable bycatch determined at this time. However, given having no impact on the short term species. In Argentina, in the 1990s, the intense year-round fishing pressure abundance of a population. This limited angel sharks were considered from trawl and gillnet fisheries within inter-population exchange reduces the commercially important bycatch, the very restricted range of this rare recovery potential for the depleted and particularly in the Necochea school species, combined with the species’ small local populations and may shark (Galeorhinus galeus) gillnet presumed low reproductive output, it is increase the risk of local extirpations, fishery, and between 1992 and 1998, likely that S. argentina is experiencing possibly leading to complete extinction. landings of angel sharks in Argentina continued population declines Given the lack of evidence of abundant were fairly stable. However, declines in throughout its range, which is populations outside of southern Brazil, CPUE over this time period (of up to 58 significantly contributing to its and the limited connectivity between percent) were recorded for vessels extinction risk. the populations of southern Brazil and operating on the Argentine shelf, populations elsewhere throughout the indicating a level of fishing mortality on Growth Rate/Productivity species’ range, conservation of the the angel shark population that was There is limited information regarding southern Brazilian populations of S. leading to declines in abundance, and the growth and reproduction of the argentina is likely critical for the since 1998, landings have been on a Argentine angel shark, and information conservation of the taxon as a whole. decline (Massa et al. 2004b). In on natural mortality rates or the Thus, based on the available Uruguay, catches of angel sharks potential intrinsic rate of population information, low dispersal rates among (Squatina spp) have actually been on an increase for the species is unavailable. populations of S. argentina poses a increasing trend since the 1970s, and The species has an estimated maximum significant risk of extinction to the exceeded the catch limit imposed in the total length of 138 cm with a size at species. AUCFZ for 2012 (2,600 mt). However, in sexual maturity of 120 cm TL, which both Argentina and Uruguay, Argentine means the species must grow to Diversity angel sharks are relatively rare, with the approximately 87 percent of its The loss of diversity can increase a majority of angel shark landings maximum size before reaching sexual species’ extinction risk through comprised of S. guggenheim. As such, it maturity. Gravid females and neonates decreasing a species’ capability of is unclear whether overutilization is are rarely found, so little is known about responding to episodic or changing significantly contributing to the species’ the gestation and birth of this species; environmental conditions. This can extinction risk in this portion of its however, litter sizes range from 7–11 occur through a significant change or range. pups (with 9–10 pups being common) loss of variation in life history Off southern Brazil, angel sharks have and their reproductive cycle is characteristics (such as reproductive been and continue to be heavily reportedly at least biennial (Vooren and fitness and fecundity), morphology, exploited by the trawl and gillnet Chiaramonte 2006). These reproductive behavior, or other genetic fisheries (see the S. guggenheim characteristics suggest the species has characteristics. Although it is unknown assessment for more details). This heavy relatively low productivity, similar to if S. argentina has experienced a loss of exploitation has led to observed other elasmobranch species, which has diversity, the significant decline declines in the abundance of S. likely hindered its ability to quickly estimated for the population in southern argentina on the Plataforma Sul as a rebound from threats that decrease its Brazil, as well as the likely small result of recruitment overfishing abundance (such as overutilization) and populations elsewhere throughout its (primarily by the bottom gillnet fishery renders the species more vulnerable to range, and limited connectivity of these targeting monkfish). Given the natural extinction. In addition, similar to its populations, suggest the species may be rarity and low productivity of the congener S. guggenheim, S. argentina is at an increased risk of inbreeding species, these declines (of up to 80 thought to have cloacal gestation during depression or random genetic drift and percent) have placed the Argentine the latter half of pregnancy, which could experience the fixing of recessive angel shark at an increased risk of increases the likelihood that the species detrimental genes, reducing the overall extinction from stochastic and will abort pups upon capture and fitness of the species. depensatory processes. In addition, it is significantly decreases their already low likely that the population of Argentine Threats Assessment reproductive output. angel shark has continued to decline The primary threat to S. argentina is (from the 80 percent estimate in 2002) Spatial Structure/Connectivity overutilization by commercial fisheries, as a result of the continued exploitation The Argentine angel shark has a very with particular vulnerability to trawl of the species by the monkfish gillnet restricted range, from Santa Catarina, and bottom gillnet fisheries. As fishery that continued unabated until Brazil to northern Argentina (i.e., previously mentioned, the vast majority 2004, and the present fishing pressure Buenos Aires). Currently, there is no of fisheries information on angel sharks by the reduced monkfish fishery and the evidence of abundant populations is documented as ‘‘Squatina spp’’ other oceanic gillnet fisheries operating outside of southern Brazil. Argentine throughout Brazil, Uruguay, and within the species’ habitat. Further, few angel sharks are sedentary, territorial, Argentina; therefore, determining the existing regulations appear adequate to

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control the overutilization of S. the Argentine angel shark is relatively extinction risk faced by the species or argentina. In the monkfish fishery, rare outside of southern Brazil, where otherwise alter its current status. We which catches significant amounts of small, isolated populations have therefore propose to list the Argentine Argentine angel shark as byatch, a experienced substantial declines and angel shark as an endangered species. management plan was implemented in remain at risk from overutilization by Graytail Skate (Bathyraja 2005. Though the monkfish fishery has fisheries targeting deep-water monkfish. griseocauda been significantly reduced in terms of Best available information indicates the ) overall effort through catch limits and species has experienced at least an 80 Species Description fisheries restrictions, enforcement of percent reduction of its critically The graytail skate, Bathyraja management rules has been poor with important southern Brazil population as griseocauda, is a member of the genus no evident signs of recovery for this a result of intense year-round fishing Bathyraja, the most speciose genus of overexploited resource (Perez et al. pressure, and will continue to decline the family Arhynchobatidae 2009). Additionally, in 2004, the without adequate protection from (McCormack et al. 2007). Physical Argentine angel shark was classified as overutilization. Given the species’ features of the graytail skate include a ‘‘critically endangered’’ on Brazil’s restricted range and present rarity disc that is rhomboidal in shape endangered species list, which throughout the range, combined with its effectively prohibited the catch of this limited movement and dispersal (Bizikov et al. 2004), brownish in color species. However, for the most part, between populations and low with traces of darker spots or rings on there is reportedly minimal control of reproductive output, S. argentina is its dorsal surface, and white or yellow the fisheries operating on the Plataforma likely strongly influenced by stochastic coloring on the ventral side (Norman Sul, and this regulation does not or depensatory processes. This 1937; Bigelow and Schroeder 1965). The address the threat of bycatch-related vulnerability is further exacerbated by posterior margins of the pelvic and mortality of the species. Additionally, the present threats of overutilization pectoral fins are dusky, and the tail is although landings of the species are and inadequacy of existing regulatory grayish brown in color (Norman 1937), currently prohibited, the fleets’ measures that are and will continue to with the underside covered in dark extensive operations will continue to significantly contribute to the decline of spots (Bizikov et al. 2004). The dorsal contribute to the fishing mortality of all the existing populations (based on its surface is covered in numerous small life stages of the species as the demographic risks), compromising the spinules, but the tip of the snout and Argentine angel shark likely has high species’ long-term viability. Therefore, axils of the pectoral fins lack spinules discard mortality rates based on rates based on the best available information (Bigelow and Schroeder 1965). There estimated for similar angel shark species and the above analysis, we conclude are 18–20 strong median spines on the (see spiny angel shark—Threats that S. argentina is presently at a high tail that begin above the origin of the Assessment). Thus, given general risk of extinction throughout its range. pelvic fins and extend to the first dorsal similarities between the Argentine angel fin (Norman 1937; Springer 1971; Protective Efforts shark and other Squatina species, it Bizikov et al. 2004). Males have alar seems reasonable to infer similar Aside from the management goals thorns, curved spines on the outer part discard survival rates for the Argentine outlined in the previously described of their pectoral fins, arranged in rows angel shark from these other Squatina FAO NPOA-sharks in Uruguay, we with 5–7 thorns per row (Bizikov et al. species. As such, given the sensitive life could not find any additional 2004). information regarding protective efforts history traits of the Argentine angel Range and Habitat Use shark as well as the evidence of for the Argentine angel shark. The graytail skate occurs in significant population declines, an Proposed Determination assumed 60 percent at-vessel mortality Southwest Atlantic waters off the coasts rate in trawl fisheries and 25–67 percent Based on the best available scientific of Argentina, Uruguay, Chile, and the mortality in gillnets is likely to and commercial information as Falkland Islands, and in the Southeast significantly contribute to the presented in the status review report Pacific off of Chile (Sa´ez and Lamilla overutilization of the species and and this finding, we find that the 2004). They have been caught at ° increase its extinction risk. Argentine angel shark is presently at latitudes as far north as 39 S. in the Overall, it is likely that S. argentina risk of extinction throughout all of its Pacific Ocean and 34° S. in the Atlantic has suffered significant population range. We assessed the ESA section Ocean, and as far south as 60° S. in the declines throughout its restricted range 4(a)(1) factors and conclude that the Southern Ocean on the Antarctic shelf as a result of historical and continued species faces ongoing threats from (Bigelow and Schroeder 1965; Figueroa overutilization of the species from direct overutilization and inadequacy of et al. 1999; Sa´ez and Lamilla 2004). A and indirect fishing pressure. Given the existing regulatory mechanisms few individuals have been captured on reduction of the species’ critically throughout its range. The species’ the Antarctic continental shelf, around important southern Brazilian population present rarity and restricted range, the Antarctic Peninsula. There are also of at least 80 percent, combined with combined with the its natural biological unconfirmed records of graytail skate in inadequate regulatory mechanisms in vulnerability to overexploitation and the Southern Ocean in Prydz Bay, this part of the species’ range to control demographic risks (e.g., low and Antarctica (GBIF 2013). If these records the high level of fishing pressure on the declining abundance, low productivity, are validated, this would extend the species, we conclude that likely small and/or isolated populations range of the skate beyond the southwest overutilization is significantly at an increased risk of random genetic Atlantic Ocean and eastern Pacific. drift, and limited dispersal capabilities) contributing to the species’ risk of Diet and Feeding extinction. are exacerbating the negative effects of the aforementioned threats, placing this Various studies on graytail skate diet Risk of Extinction species in danger of extinction. We also indicate they are opportunistic Although there is significant found no evidence of protective efforts predators that consume a variety of prey uncertainty regarding the current for the conservation of Argentine angel items, but primarily favor fish. The most abundance of the species, it appears that shark that would reduce the level of extensive study of the diet and feeding

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habits of the graytail skate caught of 14 years for males and 17.8 years for stenothermic and stenohaline behavior. around the Falkland Islands found that females. Based on commercial fleet In other words, the species appears to skates smaller than 50 cm (DW) preyed observer and research cruise data tolerate very narrow ranges of mostly on benthic gammarid amphipods collected around the Falkland Islands, temperature and salinity (Figueroa et al. and isopods, such as Serolis spp., males reached 50 percent maturity at a 1999), with catch data that suggest that whereas skates larger than 50 cm DW disc width of 76–77 cm (Agnew et al. the species occurs at water temperatures preyed increasingly on fishes (Brickle et 2000; Wakeford et al. 2005). A Falkland below 6 °C (Menni and Lopez 1984; al. 2003). Subsequent studies off the Islands study of graytail skate suggests Colonello and Massa 2004) and salinity Falkland Islands have confirmed this that graytail skate females may spawn above 33.9 psu (Colonello and Massa ontogenetic diet shift (Laptikhovsky et year-round with a weak spawning peak 2004). al. 2005). In adult graytail skate, fish can in the spring and summer months Throughout their range, graytail make up more than 40 percent of the observed (Arkhipkin et al. 2008). skates are found at depths between 106 diet (Sa´nchez and Mabragan˜ a 2002). Off Around the Falkland Islands, the m and 1,010 m, but have been caught as the coast of Argentina, the graytail skate spawning grounds of the graytail skate shallow as 77 m in Argentine waters did not consume crustaceans (Sa´nchez can be found northwest of the islands in (Bu¨ cker 2006). Graytail skate are and Mabragan˜ a 2002), which contrasts deep waters, close to the edge of the typically most common at depths below with data from the Falkland Islands. continental shelf between 200 and 300 300 m (Bigelow and Schroeder 1965; m deep (Arkhipkin et al. 2008) and in Menni and Lopez 1984; Brickle et al. Growth and Reproduction waters south of 51° latitude (Dr. 2003; Laptikhovsky et al. 2005; Graytail skates have a lifespan of Andreas Winter, Falkland Islands Wakeford et al. 2005; Arkhipkin et al. approximately 28 years, with a Fisheries Stock Assessment Scientist, 2008; Arkhipkin et al. 2012). However, maximum observed disc width of 130 personal communication 2015). Based in Argentina, the highest density of cm and a maximum weight of 30.4 kg on catches of the smallest skates, it is graytail skate catches was reported at (Arkhipkin et al. 2008; Wakeford et al. thought that hatchlings have disc depths of 120 m on the Argentina 2005). Based on vertebral band counts widths between 9 cm and 12 cm platform between 45° S. and 41° S. from samples collected from along the (Brickle et al. 2003; Arkhipkin et al. during the late winter and early spring coast of Argentina, Bu¨ cker (2006) 2008). months (Colonello and Massa, 2004). As calculated the relative growth rate (k) graytail skates mature, they display an from the von Bertalanffy growth Genetics and Population Structure ontogenetic shift in depth preference equation to be 0.064 year¥1 with a Studies examining the genetics of the (Arkhipkin et al. 2008). For example, in theoretical maximum size (L∞) of 169.9 species or information on its population Falkland Islands waters, hatchlings cm TL and an estimated size-at-birth structure could not be found. occupy nursery grounds of (L0) of 6.1 cm. Arkhipkin et al. (2008), approximately 300 m–350 m depth, but Demography using samples collected only off the transition to deeper waters of 400 m– Falkland Islands, reported a lower Little is known about the population 600 m as juveniles (Arkhipkin et al. growth rate (k) of 0.02 year¥1, with a growth and natural mortality of the 2008). At 20 cm–30 cm DW, some maximum theoretical size (L∞) of 313.4 graytail skate. However, based on the individuals migrate up to shallower cm total length. Growth rates of graytail life history parameters described depths of 200 m–400 m, while others skate begin around 5.6 cm/year for the previously, like other elasmobranchs, move into water deeper than 600 m first 9 years of life and decline to 4.3 the graytail skate is a K-selected species (Arkhipkin et al. 2008). Skates 80 cm– cm/year between 14 and 20 years old with slow growth rates and late age at 90 cm DW or larger occur most (Arkhipkin et al. 2008). In comparison, maturity, which is indicative of low commonly at depths of 400 m–600 m a study of caudal thorn band counts and productivity (Gallagher 2000; Bu¨ cker (Arkhipkin et al. 2008). Despite these vertebral centra ring counts found that 2006; Arkhipkin et al. 2008). depth changes, studies around the the most accurate von Bertalanffy Historical and Current Distribution and Falkland Islands have shown little growth parameters came from the Population Abundance evidence of large spatial or temporal vertebral centra with the relative growth movements, which could indicate that rate (k) based on vertebrae centra to be Graytail skate occur on the graytail skates carry out their entire life 0.033 year¥1 with a theoretical continental shelf and slope in the cycle within the waters where they maximum size (L∞) of 219.7 cm total southwestern Atlantic Ocean, south of hatch (Agnew et al. 2000; Wakeford et ° length (Gallagher 2000). However, based 34 S. and in the southeastern Pacific al. 2005; Winter et al. unpublished). on observed size data, these parameters Ocean, south of 39° S. (Figueroa et al. Range-wide abundance estimates for still slightly underestimate growth 1999; Sa´ez and Lamilla 2004). In the graytail skate are not available; however, (Gallagher 2000). Falkland Islands, graytail skate are biomass estimates exist for the Little is known about the caught in cool, deep waters on the populations off the Falkland Islands and reproduction of the graytail skate slopes of the continental shelf break, Argentina. In the Falkland Islands, (Sa´nchez and Mabragan˜ a 2002) and making them more common to the west graytail skate were part of the fish available age and growth studies from of the islands (Agnew et al. 1999; assemblage of both the southern and the same region provide conflicting Arkhipkin et al. 2008; Arkhipkin et al. northern skate and ray stocks. They estimates for length and age at maturity. 2012). Outside the Falkland Islands, on were particularly abundant south of the For example, in the Falkland Islands, the Patagonian shelf, they are more islands, making them dominant in Gallagher (2000) estimated a total length commonly found on the northwestern catches of the southern skate and ray at 50 percent maturity of 120.7 cm for outer shelf and northern shelf and slope assemblage. However, due to declining both sexes, with males and females (Figueroa et al. 1999; Arkhipkin et al. CPUEs of the southern stock, especially maturing after 17.6 and 24.8 years 2012). In Argentina, graytail skate are for graytail skate, the southern rajid respectively. Arkhipkin et al. (2008) found on the continental shelf and slope fishery was closed in 1996 (Agnew et al. estimated a total length at 50 percent around Argentina south of 37° S. and 1999; Agnew et al. 2000; Wakeford et al. maturity to be 108.2 cm for females and 41° S. respectively (McCormack et al. 2005). Current biomass estimates from 94.5 cm for males, with age at maturity 2007), where they exhibit strict this area could not be found. North of

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the Falkland Islands, declines in the Summary of Factors Affecting the are most heavily exploited in the CPUE of graytail skate were also Graytail Skate Falkland Islands multispecies skate and observed between 1992 and 2001 We reviewed the best available ray fishery by foreign fleets (Agnew et (Wakeford et al. 2005); however, based information regarding historical, al. 1999; Falkland Islands Government on recent biomass estimates, the current, and potential threats to the 2005–2013). Prior to the 1990s, catches population appears to have recovered graytail skate species. We find that the from the Falkland Islands were mainly and stabilized. Specifically, analysis of main threat to this species is attributed to Spanish vessels fishing in 2010 fishery survey cruise data resulted overutilization for commercial a mixed groundfish fishery, with rajid in an estimated biomass of graytail skate purposes; however, we consider the catches of less than 1,500 t per year of 7,232 t, which is consistent with the severity of this threat to be greatly (Wakeford et al. 2005). However, in earlier biomass estimates for the species reduced by the regulatory mechanisms 1989, Korean vessels began to from the 1990s (Falkland Islands in place in the Falkland Islands, where specifically target rajids in this fishery Government 2011). As this biomass the species was historically most using demersal trawls, and by 1991 estimate is just for the graytail skate heavily exploited. Thus, we find that catches of skates and rays rose to more population north of the Falkland historical and present levels of than 7,000 t/year (Wakeford et al. 2005). Islands, it is likely a significant utilization are not exceeding the Subsequently, two rather distinct rajid underestimation of the total biomass for species’ biological capacity to sustain fisheries developed within the Falkland the entire Falkland Islands population, current levels of exploitation. We also Islands: a southern rajid fishery that especially considering the southern find that current regulatory measures fished in a small area south of the stock, which was historically more are adequate to protect the species from Falkland Islands (a ray ‘‘hot spot;’’ abundant, has been protected from further overutilization. Additionally, Agnew et al. 2000), and a northern rajid targeted fishing since 1996. available information does not indicate fishery that operated in a more In 2002, Sa´nchez and Mabragan˜ a that habitat destruction or modification, extensive area to the north of the (2002) estimated the population disease, predation or other natural or Falkland Islands (primarily on the slope abundance of the graytail skate on the manmade factors are operative threats between 200 m–400 m depths; continental Argentine shelf between 48° Wakeford et al. 2005). In the 1990s, the ° on these species. We summarize S. and 55 S. to be 259,210 individuals, information regarding these factors and graytail skate was the most important or 2,431.98 t. This estimate was their interactions below according to species caught in the Falkland Islands calculated prior to the apparent section 4(a)(1) of the ESA. See multispecies rajid fisheries based on recovery of the graytail skate in the Casselbury and Carlson (2015g) for a catch weight, and was estimated to Falkland Islands and also corresponds more detailed discussion of these make up approximately 58 percent of to when CPUE of the graytail skate was factors. the catch in the southern rajid fishery at its minimum in the Falkland Islands and 39 percent of the catch in the (Wakeford et al. 2005). As such, it could Present or Threatened Destruction, northern rajid fishery between 1993 and be assumed that biomass has since Modification, or Curtailment of Habitat 1995 (Agnew et al. 1999; Bizikov et al. increased on the shelf; however, with no or Range 2004). However, with this heavy recent abundance estimates available, Trawl fisheries occur throughout the exploitation on the skate populations by the trends within this portion of the graytail skate’s range. Studies show that Korean fleets (which were responsible species’ range cannot be determined the interaction of bottom trawling gears for 88 percent of the directed rajid catch with certainty. with bottom substrate can have negative between 1990 and 1997; Agnew et al. Farther north on the Argentine shelf, effects on benthic fish habitat 2000), the proportional catches of between 45° S. and 41° S., the biomass (Valdemarsen et al. 2007). These graytail skate declined in all areas that of graytail skate was estimated to be 503 impacts are often the most serious on were fished. This decline was t in 2004, but had a large confidence hard substrates with organisms that particularly precipitous in the southern interval (±2,237 t), with an average grow up from the bottom, such as corals batoid aggregation area, where graytail density of the species of 0.05 t/nm2 and sponges, but alterations to soft skate spawn (A. Winter, pers. comm. (Colonello and Massa 2004). More substrates have also been seen. The 2015) and had previously comprised the recent estimates or trends in population trawl doors on bottom otter trawls often majority of the catch (Agnew et al. abundance or biomass levels for graytail cause the most damage to the ocean 1999). Agnew et al. (2000) calculated skate are not available. bottom, but other parts of trawling gear, that total mortality rates (fishing There is very little information such as weights, sweeps, and bridles mortality rates + natural mortality rates) pertaining to the presence of graytail that contact the bottom can also be in the northern and southern areas were skate in Uruguayan and Chilean waters. damaging. Intense fishing disturbance significantly higher than what could be No information on commercial, from trawling has reduced the sustained by the batoid assemblage, recreational, or research catches of abundance of several benthic species particularly graytail skates. Specifically, graytail skate is available from Uruguay. (Valdemarsen et al. 2007); however, the authors estimated that graytail Likewise, there is no estimate of there is no specific information skates could sustain total mortality rates abundance from this area. In Chile, available that indicates this habitat of less than 0.3/year; however, the total graytail skate are found south of 41° S. modification has had a direct effect on mortality rate in the northern area from and at depths of 137 m to 595 m the abundance of the graytail skate, or 1991–1995 was on the order of 0.42/year (McCormack et al. 2007). In 1995, Saez is specifically responsible for the and in the southern area was 0.61/year and Lamilla (2004) caught 42 graytail curtailment of its habitat or range. (Agnew et al. 2000). Consequently, skate between March and December at significant declines in CPUE were 350 m depth approximately 20 miles Overutilization for Commercial, observed between 1990 and 1997. A from Punta Galera; however, no other Recreational, Scientific, or Educational steep 58 percent decline was noted in information is available on scientific or Purposes the southern rajid fishery from 1993 to commercial catch distribution or Information available on the harvest 1996, which was attributed to the population abundance from this area. of the graytail skate indicates that they decline in graytail skate abundance

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

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well as the lack of species-specific S, which effectively closed the southern under Uruguay’s FAO NPOA-sharks, information and trends data makes it ray fishery. Before the prohibition, which outlines plans to: investigate the difficult to determine the magnitude of graytail skate were particularly species’ age, growth, reproduction, diet, utilization that may be occurring abundant south of the islands, where its distribution, and habitat use in specifically for B. griseocauda in this spawning grounds are mostly located Uruguayan waters; generate a time part of its Argentinian range, and (A. Winter, pers. comm. 2015), and series for catch and effort of the skate in whether this level of utilization is made up a significant portion of the fisheries; conduct an abundance contributing significantly to the species’ catch from this area. Thus, this measure assessment; establish measures to extinction risk. helps protect not only a large segment review current fishing licenses for Similarly, little information is of the population from further depletion graytail skate and determine possible available on the exploitation of the in an area where they were historically modifications to the licenses; and graytail skate in Chilean waters. There most concentrated, but also important finally, prohibit new fishing permits. is a directed skate fishery off Chile that life history behavior required for the However, aside from the species’ primarily targets the yellownose skate survival of the species (Agnew et al. presence in Uruguayan waters, there is (Zearaja chilensis), and although 2000). In addition to the closure of the a significant lack of information information on the depth at which the southern ray fishery via the trawl regarding the status of graytail skate in fishery operates could not be found, Z. prohibition, catch limits were also Uruguay; thus, there is no indication chilensis lives at depths between 28 m imposed for the northern rajid fishery in that existing regulatory mechanisms are and 435 m. This depth range overlaps 1996. Since then, the northern batoid inadequate in controlling threats to the with the shallower half of the graytail stock has seen a gradual increase in both species in this portion of its range, or skate’s depth range (Kyne et al. 2007) CPUE and biomass, with total catches are contributing significantly to its risk and thus this fishery may also lower than MSY, suggesting regulatory of extinction. incidentally catch graytail skates. Since measures are adequate in providing for In Chile, there are little to no 1979, declines in Z. chilensis catches the sustainable exploitation of the regulations for the protection of graytail have been reported, and it is suspected northern skate assemblage in Falkland skate; however, the exploitation of the that other skate species, including the waters. Data also suggest that these species in Chilean waters is minimal. graytail skate, have also been affected regulatory measures have allowed for While there are regulations pertaining to (McCormack et al. 2007); however, the recovery of the graytail skate other fisheries in Chilean waters that graytail skate comprise less than 5 population, as indicated by the overlap the graytail skate’s range, it is percent of the skate landings in this increasing CPUE and sizes of graytail unknown how these regulations affect fishery (McCormack et al. 2007). As skate in recent catches. As such, the the status of graytail skate. Based on the such, the impact of this fishery on Fisheries Committee, which advises the available information, there is no graytail skate abundance and overall Falkland Islands Fisheries Department, indication that existing regulatory extinction risk is likely to be minimal. recommended maintaining the skate mechanisms are inadequate in Disease or Predation target catch at the current level of effort controlling threats to the species in this allocation for the 2016 fishing year as portion of its range, or are contributing At this time, there is no available these limits are effective at maintaining significantly to its risk of extinction. information regarding diseases or a sustainable multispecies fishery and Other Natural or Manmade Factors predators of the species. As such, there appear adequate to protect the graytail Affecting the Species is no evidence to indicate that these skate from extinction. factors are a threat to the graytail skate. In Argentina, the graytail skate is Besides the information already Inadequacy of Existing Regulatory covered under the country’s FAO discussed above in the other factor Mechanisms NPOA-sharks; however, it is not sections, no additional information was considered a priority species. Several found regarding threats to the species In the Falkland Islands, there are sources have noted that Argentina does that would fall under this category. As numerous management measures in little to actively protect elasmobranchs, such, there is no evidence to indicate place that provide for the protection of particularly skates and rays, in its that this factor is a threat to the graytail graytail skate from overutilization. The waters (Massa and Hozbor 2003; Massa skate. Falkland Islands multispecies fishery, et al. 2004b, McCormack et al. 2007). Extinction Risk where graytail skate is presumably most Though total allowable catch, minimum heavily exploited, is rigorously managed sizes, and annual quotas are in place for Demographic Risk Analysis through fishing effort controls. In order many elasmobranchs in Argentina, they Abundance to protect the southern batoid are largely ignored and poorly enforced aggregation area that displayed marked (McCormack et al. 2007). In 2013, El Although range-wide abundance declines in CPUE in the early 1990s Instituto Nacional de Investigacio´n y estimates for graytail skate are (Agnew et al. 1999), the Falkland Desarrollo Pesquero (INIDEP) set the unavailable; biomass estimates and Islands government implemented a recommended total allowable catch for trends exist for the areas where the number of management measures to all skates and rays at 9,000 t and a species was historically and is currently ensure long-term sustainability of the landing limit for skates and rays was set most abundant. In the Falkland Islands, rajid fishery, including: (1) The at no more than 30 percent of the catch. graytail skate represented a dominant placement of observers on vessels to However, due to the lack of information part of the southern rajid assemblage in identify batoids to species and collect regarding the status of the graytail skate the mid-1990s and comprised around 39 other biological data to inform fisheries in Argentina, there is no indication that percent of the northern rajid catch. Due management; (2) the development of existing regulatory mechanisms are to heavy fishing pressure contributing to specific skate and ray fishery seasons inadequate in controlling threats to the unsustainable mortality rates, and licenses to better regulate the catch species or are contributing significantly significant declines in the CPUE of the of rajids; and (3) the implementation to the species’ risk of extinction. species were observed between 1992 and continuation of a prohibition on In Uruguay, the graytail skate is and 2007 indicating a likely reduction trawling for skates and rays south of 51° considered a species of high priority in population abundance. However,

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since the decline, CPUE (as an index of instantaneous per capita growth rate of batoid stock assemblage. As for graytail abundance of graytail skate) from north a species. However, since 2006, data skates specifically, they remain one of of the Falkland Islands has been from the Falkland Islands Government the most abundant species caught in the increasing, already reaching levels show an increase in size of the modal Falkland Islands multispecies skate observed in 1997–2001, with biomass of disc width of graytail skate catches, fishery. Recent data from the Falkland the species in 2010 estimated to be with the most recent size estimate of 63 Islands Government shows an 7,232 t, consistent with biomass cm in 2012, likely indicating that the increasing trend in the CPUE of the estimates from the early 1990s. population is recovering and that species as well as in the the modal disc Additionally, the graytail skate remains growth rate is no longer declining. width of graytail skate catches, with the one of the most abundant species caught latest estimate of 63 cm DW in 2012. Spatial Structure/Connectivity in the Falkland Islands multispecies While 63 cm is still below the size of skate fishery. Therefore, while the Based on trends in commercial sexual maturity (i.e., 75 cm) it is a species likely experienced historical fisheries data from the Falkland Islands marked improvement from the modal declines in abundance as a result of and Argentina, Wakeford et al. (2005) disc widths between 1993 and 2006 heavy exploitation in the early 1990s, concluded that graytail skates have (after heavy exploitation), which ranged the available information on biomass limited spatial and temporal movements between 25 cm and 40 cm, and indicates estimates and trends between the 1990s and, therefore, may likely exist as potential recovery of the population. and 2014 indicate that the population is localized populations. Limited inter- Additionally, since the early 2000s, potentially stabilized and even population exchange reduces the there has been a general decreasing recovering. Therefore, the species’ recovery potential for depleted and trend in the targeting of skate and ray present level of abundance is unlikely to small local populations and may species in the Falkland Islands, with pose a demographic risk to the species. increase the risk of local extirpations, most species now taken as bycatch in Furthermore, there is no other possibly leading to complete extinction. the finfish fishery. Furthermore, total abundance information or trend data However, no other information is skate catch in recent years has remained from the rest of the species’ range to available regarding spatial structure or below MSY, indicating that current indicate that the species’ present connectivity of graytail skate catch and effort of the skate and ray abundance level is contributing populations throughout its range, and fishery are likely sustainable. Based on significantly to its risk of extinction. there is no evidence to suggest this the above information, it is clear that demographic risk is presently existing regulatory measures, including Growth Rate/Productivity significantly contributing to the graytail current catch limits and trawling Relative growth rates (k) of graytail skate’s risk of extinction. closures, are adequate to protect the skates were estimated to be 0.064 year¥1 Diversity graytail skate in the Falkland Islands in Argentinean waters (i.e., low), and from extinction. 0.02 year¥1 to 0.033 year¥1 in the The loss of diversity can increase a In Argentina, there is an active Falkland Islands (i.e., very low). species’ extinction risk through commercial elasmobranch fishery, Graytail skates are long-lived species, decreasing a species’ capability of which exploits sharks, skates, and rays, with an estimated lifespan of responding to episodic or changing and it has shown an increasing trend in approximately 28 years, and a environmental conditions. This can both catches and number of vessels maximum disc width of 130 cm. occur through a significant change or reporting skate and ray landings (Massa Although age and growth studies from loss of variation in life history and Hozbor 2003). However, based on skates in the same region provide characteristics (such as reproductive the lack of species-specific information conflicting estimates for length and age fitness and fecundity), morphology, from the region, it is highly uncertain if at maturity, with age of maturity behavior, or other genetic present levels of utilization of skates estimates ranging from 14–17.6 years for characteristics. Currently, there is no and rays are a threat that is contributing males and 17.8–24.8 years for females, information regarding the graytail significantly to the extinction risk of the all estimates indicate a very late age of skates’ diversity throughout its range, graytail skate. maturity. While there is some evidence thus we can not conclude whether its In Chile, a directed skate fishery that to suggest that graytail skates may present level of diversity is contributing primarily targets Zearaja chilensis in reproduce year-round, overall, these to its extinction risk. areas where graytail skate may also reproductive characteristics suggest the occur has reported declines in catch Threats Assessment species has relatively low productivity, since 1979. It is suspected that other similar to other elasmobranch species, The best available information skate species, including the graytail which may hinder its ability to quickly indicates that graytail skates are most skate, have also been affected. However, rebound from threats that decrease its heavily exploited in the Falkland there are no available data that indicate abundance (such as overutilization) and Islands multispecies skate and ray a decline in graytail skate abundance or render the species more vulnerable to fishery by foreign fleets and likely catch, and given that the species extinction in the face of other suffered significant declines in comprises less than 5 percent of the demographic risks and threats. abundance due to overexploitation in total skate landings in this fishery, it is Additionally, the observed decrease in the early 1990s. However, since 1996, unlikely that this fishery is significantly the species’ mean disc width in catches the area of operation of the Falkland contributing to the extinction risk of the from 1993–1995 and 1997–2006 (to Islands rajid fishery has been graytail skate. sizes that ranged between 25 cm and 40 significantly restricted (to an area north Overall, while the species likely cm) likely portended a declining growth of the Islands) with imposed catch experienced historical declines in rate for the species. This is because limits to manage the northern batoid abundance during the 1990s due to changes in metrics, such as average size, stock assemblage (which includes exploitation by the Falkland Islands can significantly impact other important graytail skates) within this area. As a multispecies rajid fisheries, the life history functions, like fecundity or result of these management measures, available biomass estimates and trends even natural mortality rates there has been a gradual increase in over the past decade, including gradual (Audzijonyte et al. 2015), that affect the CPUE and biomass of the northern increases in the CPUE and biomass of

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the northern batoid stock and analysis, we conclude that B. endangered or threatened there; if we specifically the graytail skate in recent griseocauda is at a low risk of extinction determine that the species is not years, as well as an increasing trend in throughout its range, and as such, does endangered or threatened in a portion of graytail modal disc width size, indicate not warrant listing as a threatened or its range, we will not need to determine the population is potentially stable and endangered species throughout its if that portion was ‘‘significant.’’). Thus, possibly moving towards recovery. This range. if the answer to the first question is is likely a result of rigorous regulations negative—whether that regards the Significant Portion of Its Range Analysis implemented by the Falkland Islands significance question or the status government to sustainably manage the Because our range-wide analysis for question—then the analysis concludes rajid fishery by reducing fishing effort, the species leads us to conclude that the and listing is not warranted. accomplished by setting catch limits in species is not threatened or endangered After a review of the best available the northern rajid fishery and closing throughout its range, under the final information, we identified the Falkland the southern rajid fishery area, where Significant Portion of Its Range (SPR) Islands as likely constituting a graytail skates likely spawn and were policy announced in July 2014, we must ‘‘significant’’ portion of the graytail historically most heavily exploited. It go on to consider whether the species skate range. Under the policy, a portion should be noted that while this closure may have a higher risk of extinction in of a species’ range is significant if, helps to protect the Falkland Islands a significant portion of its range (79 FR without that portion, the species would population, due to uncertainty 37577; July 1, 2014). have an increased vulnerability to surrounding the connectivity of graytail The final policy explains that it is threats to the point that the overall skate populations, these regulations may necessary to fully evaluate a portion for species would be in danger of extinction not provide protection to skate potential listing under the ‘‘significant or likely to become so in the foreseeable populations found outside of Falkland portion of its range’’ authority only if future. As mentioned previously, the waters. However, based on the available information indicates that the members historical and current fisheries data information, it appears that the Falkland of the species in a particular area are indicate that graytail skate are likely Islands is where the species is most likely both to meet the test for biological most concentrated in Falkland waters. concentrated, and, hence, the protection significance and to be currently Graytail skate have also been identified of this population from extinction is endangered or threatened in that area. and caught elsewhere throughout its likely critical for the survival of the Making this preliminary determination range, such as north of the Falkland species. Outside of the Falkland Islands, triggers a need for further review, but Islands on the Argentinian shelf the minimal available information on does not prejudge whether the portion between 45° S. and 41° S., and on the the species does not indicate that actually meets these standards such that Pacific coast off Chile (south of 41° S.); present levels of utilization or any other the species should be listed: however, based on trends in commercial factors are contributing significantly to To identify only those portions that fisheries data from the Falkland Islands the extinction risk of the species. warrant further consideration, we will and Argentina, Wakeford et al. (2005) determine whether there is substantial concluded that graytail skates have Risk of Extinction information indicating that (1) the limited spatial and temporal movements While the species’ demographic portions may be significant and (2) the and, therefore, may likely exist as characteristics increase its inherent species may be in danger of extinction localized or isolated populations. If we vulnerability to depletion, and likely in those portions or likely to become so assume the Falkland Islands population contributed to past population declines within the foreseeable future. We is isolated from the populations of of varying magnitudes, the best emphasize that answering these graytail skate elsewhere throughout its available information suggests these questions in the affirmative is not a range, then, technically, loss of this risks have decreased due to the determination that the species is population would not directly affect the adequate control of exploitation of the endangered or threatened throughout a abundance of the other remaining species. In the Falkland Islands, where significant portion of its range—rather, populations. However, loss of this the species was most heavily exploited it is a step in determining whether a population could significantly increase and is likely presently most more detailed analysis of the issue is the extinction risk of the species as a concentrated, abundance estimates and required (79 FR 37586, July 1, 2014). whole, as only small, fragmented, and trends from the 1990s to 2013, and Thus, the preliminary determination isolated populations of the species increases in the species’ mean disc that a portion may be both significant (based on the best available abundance width, suggest potential stabilization and endangered or threatened merely information—see the Historical and and even recovery of the population. requires NMFS to engage in a more Current Distribution and Population The continued rigorous management detailed analysis to determine whether Abundance and Demographic Risk and monitoring of the fishery appears the standards are actually met (Id. at Analysis sections above) would remain, adequate in protecting the species from 37587). Unless both are met, listing is making them more vulnerable to levels of overutilization that would not warranted. The policy further catastrophic events and environmental increase its extinction risk. Despite explains that, depending on the or anthropogenic perturbations. Limited fishing pressure in other parts of the particular facts of each situation, NMFS inter-population exchange also reduces species’ range (e.g., Chile and may find it is more efficient to address the recovery potential for these small Argentina) and evidence of it being the significance issue first, but in other local populations and increases the risk taken as bycatch in various fisheries, cases it will make more sense to of local extirpations and overall graytail skates are not monitored and we examine the status of the species in the complete extinction. have no other information (e.g., catch potentially significant portions first. Under the policy, if we believe the rates, abundance trends, or any other Whichever question is asked first, an Falkland Islands population may species-specific data) to indicate that affirmative answer is required to constitute a ‘‘significant’’ portion of the present levels of utilization or any other proceed to the second question. Id. (‘‘[I]f range, then we must either evaluate the factors are significantly contributing to we determine that a portion of the range extinction risk of this population first to the species’ risk of extinction. Thus, is not ‘‘significant,’’ we will not need to determine whether it is threatened or considering the above information and determine whether the species is endangered in that portion or determine

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if this portion is, in fact, ‘‘significant.’’ in the northern rajid fishery of the also require Federal agencies to confer Ultimately, of course, both tests have to Falkland Islands have contributed to a with us on actions likely to jeopardize be met to qualify the species for listing. significant reduction of fishing pressure the continued existence of species Given the extremely limited amount of on the species, leading to increases in proposed for listing, or that result in the information on the species outside of its the abundance of the population and destruction or adverse modification of Falkland Islands range, it is difficult to providing for sustainable fishing of the proposed critical habitat of those conduct a more definitive analysis to northern Falkland Islands rajid species. It is unlikely that the listing of determine whether or not this portion assemblage; (4) targeting of skates and these species under the ESA will does, in fact, constitute a ‘‘significant’’ rays in the Falkland Islands, where the increase the number of section 7 portion of the range of the graytail skate. species was most heavily exploited, has consultations, because these species Additionally, there is no information to been on a decreasing trend since the occur outside of the United States and suggest that any other portion may be early 2000s; (5) there is no evidence that are unlikely to be affected by Federal significant. However, even if we were to destruction of habitat, disease or actions. assume that the Falklands Islands predation are factors contributing to an Critical Habitat population does constitute a increased risk of extinction for the ‘‘significant’’ portion of the graytail species; and (6) the continual Critical habitat is defined in section 3 skate range, based on the information implementation of rigorous monitoring of the ESA (16 U.S.C. 1532(5)) as: (1) and analysis in the previous extinction and fishery management measures in The specific areas within the risk section, there are no identified the Falkland Islands appears effective in geographical area occupied by a species, threats concentrated in this portion that addressing the most important threat to at the time it is listed in accordance are significantly contributing to the the species (overharvest) now and into with the ESA, on which are found those species’ risk of extinction. In fact, the the foreseeable future. Based on these physical or biological features (a) most recent available information findings, we conclude that the graytail essential to the conservation of the indicate that existing regulatory skate is not presently in danger of species and (b) that may require special measures are adequate in protecting the extinction throughout all or a significant management considerations or graytail skate in the Falkland Islands portion of its range, nor is it likely to protection; and (2) specific areas outside from extinction, with graytail skate become so within the foreseeable future. the geographical area occupied by a abundance on a positive trend and Accordingly, the graytail skate does not species at the time it is listed upon a exhibiting signs of population recovery meet the definition of a threatened or determination that such areas are based on both CPUE and size data. endangered species and therefore does essential for the conservation of the Thus, under the policy, the preliminary not warrant listing as threatened or species. ‘‘Conservation’’ means the use determination that a portion of the endangered at this time. of all methods and procedures needed species’ range may be both significant to bring the species to the point at Effects of Listing and endangered or threatened has not which listing under the ESA is no been met. Therefore, listing is not Conservation measures provided for longer necessary. Section 4(a)(3)(A) of warranted under the SPR policy. species listed as endangered or the ESA (16 U.S.C. 1533(a)(3)(A)) threatened under the ESA include requires that, to the extent prudent and Proposed Determination recovery actions (16 U.S.C. 1533(f)); determinable, critical habitat be Based on the best available scientific concurrent designation of critical designated concurrently with the listing and commercial information as habitat, if prudent and determinable (16 of a species. However, critical habitat presented in the status review report U.S.C. 1533(a)(3)(A)); Federal agency shall not be designated in foreign and this finding, we find that the requirements to consult with NMFS countries or other areas outside U.S. graytail skate is not presently in danger under section 7 of the ESA to ensure jurisdiction (50 CFR 424.12(h)). of extinction throughout all or a their actions do not jeopardize the The best available scientific and significant portion of its range, nor is it species or result in adverse modification commercial data as discussed above likely to become so in the foreseeable or destruction of critical habitat should identify the geographical areas occupied future. We summarize the factors it be designated (16 U.S.C. 1536); and by Isogomphodon oxyrhynchus, supporting this conclusion as follows: prohibitions on taking for endangered Rhinobatos horkelii, Mustelus fasciatus, (1) Although there is no formal estimate species (16 U.S.C. 1538). Recognition of M. schmitti, Squatina guggenheim and of the current population size and the species’ plight through listing S. argentina as being entirely outside historical declines in biomass have been promotes conservation actions by U.S. jurisdiction, so we cannot observed, current biomass estimates Federal and state agencies, foreign designate critical habitat for these from the Falkland Islands, where the entities, private groups, and individuals. species. species is likely most concentrated, The main effects of the proposed We can designate critical habitat in suggest the population is stable and endangered listings are prohibitions on areas in the United States currently CPUE trends indicate abundance is take, including export and import. unoccupied by the species, if the area(s) increasing; (2) a reduction in mean disc are determined by the Secretary to be width of the Falkland Islands Identifying Section 7 Conference and essential for the conservation of the population occurred in the late 1990s Consultation Requirements species. Regulations at 50 CFR 424.12(e) and early 2000s as a result of intensive Section 7(a)(2) (16 U.S.C. 1536(a)(2)) specify that we shall designate as fishing pressure; however, recent of the ESA and NMFS/USFWS critical habitat areas outside the evidence suggests an increase in modal regulations require Federal agencies to geographical range presently occupied disc width, which is likely indicative of consult with us to ensure that activities by the species only when the population recovery; (3) while an they authorize, fund, or carry out are not designation limited to its present range identified threat to the species was likely to jeopardize the continued would be inadequate to ensure the historical overutilization in the Falkland existence of listed species or destroy or conservation of the species. The best Islands commercial fisheries, adversely modify critical habitat. available scientific and commercial subsequent fishery closures in the Section 7(a)(4) (16 U.S.C. 1536(a)(4)) of information on these species does not southern rajid fishery and catch limits the ESA and NMFS/USFWS regulations indicate that U.S. waters provide any

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specific essential biological function for Identification of Those Activities That interested parties on information in the any of the species proposed for listing. Would Not Constitute a Violation of status review and proposed rule. Therefore, based on the available Section 9 of the ESA Comments are encouraged on these information, we do not intend to We will identify, to the extent known proposals (See DATES and ADDRESSES). designate critical habitat for at the time of the final rule, specific We must base our final determination Isogomphodon oxyrhynchus, activities that will not be considered on the best available scientific and Rhinobatos horkelii, Mustelus fasciatus, likely to result in a violation of section commercial information when making M. schmitti, Squatina guggenheim or S. 9 of the ESA. Although not binding, we listing determinations. We cannot, for argentina. are considering the following actions, example, consider the economic effects of a listing determination. Final Identification of Those Activities That depending on the circumstances, as not being prohibited by ESA section 9: promulgation of any regulation(s) on Would Constitute a Violation of Section these species’ listing proposals will take 9 of the ESA (1) Take authorized by, and carried out in accordance with the terms and into consideration the comments and any additional information we receive, On July 1, 1994, NMFS and FWS conditions of, an ESA section and such communications may lead to published a policy (59 FR 34272) that 10(a)(1)(A) permit issued by NMFS for a final regulation that differs from this requires us to identify, to the maximum purposes of scientific research or the enhancement of the propagation or proposal or result in a withdrawal of extent practicable at the time a species this listing proposal. We particularly is listed, those activities that would or survival of the species; (2) Continued possession of parts that seek: would not constitute a violation of (1) Information concerning the threats were in possession at the time of listing. section 9 of the ESA. to any of the six species proposed for Such parts may be non-commercially listing; Because we are proposing to list exported or imported; however, the (2) Taxonomic information on any of Isogomphodon oxyrhynchus, importer or exporter must be able to these species; Rhinobatos horkelii, Mustelus fasciatus provide evidence to show that the parts and Squatina argentina as endangered, (3) Biological information (life meet the criteria of ESA section 9(b)(1) history, genetics, population all of the prohibitions of section 9(a)(1) (i.e., held in a controlled environment at of the ESA will apply to these species. connectivity, etc.) on any of these the time of listing, in a non-commercial species; These include prohibitions on the activity). import, export, use in foreign (4) Efforts being made to protect any commerce, or ‘‘take’’ of the species. Protective Regulations Under Section of these species throughout their current These prohibitions apply to all persons 4(d) of the ESA ranges; (5) Information on the commercial subject to the jurisdiction of the United We are proposing to list Mustelus trade of any of these species; States, including in the United States, fasciatus and Squatina guggenheim as (6) Historical and current distribution its territorial sea, or on the high seas. threatened species. In the case of and abundance and trends for any of Take is defined as ‘‘to harass, harm, threatened species, ESA section 4(d) these species; pursue, hunt, shoot, wound, kill, trap, leaves it to the Secretary’s discretion (7) Current or planned activities capture, or collect, or to attempt to whether, and to what extent, to extend within the range of these species and engage in any such conduct.’’ The intent the section 9(a) ‘‘take’’ prohibitions to their possible impact on these species; of this policy is to increase public the species, and authorizes us to issue and, awareness of the effects of this listing on regulations necessary and advisable for (8) Information relevant to potential proposed and ongoing activities within the conservation of the species. Thus, ESA section 4(d) protective regulations the species’ range. Activities that we we have flexibility under section 4(d) to for any of the proposed threatened believe could result in a violation of tailor protective regulations, taking into species. section 9 prohibitions for these species account the effectiveness of available We request that all information be include, but are not limited to, the conservation measures. The 4(d) accompanied by: (1) Supporting following: protective regulations may prohibit, documentation, such as maps, (1) Possessing, delivering, with respect to threatened species, some bibliographic references, or reprints of or all of the acts which section 9(a) of transporting, or shipping any individual pertinent publications; and (2) the the ESA prohibits with respect to or part (dead or alive) taken in violation submitter’s name, address, and any endangered species. These 9(a) of section 9(a)(1); association, institution, or business that prohibitions apply to all individuals, the person represents. (2) Delivering, receiving, carrying, organizations, and agencies subject to transporting, or shipping in interstate or U.S. jurisdiction. We will consider Role of Peer Review foreign commerce any individual or extending some or all potential In December 2004, the Office of part, in the course of a commercial protective regulations pursuant to Management and Budget (OMB) issued activity; section 4(d) for the proposed threatened a Final Information Quality Bulletin for (3) Selling or offering for sale in species. We seek public comment on Peer Review establishing a minimum interstate commerce any part, except potential 4(d) protective regulations (see peer review standard. Similarly, a joint antique articles at least 100 years old; below). NMFS/FWS policy (59 FR 34270; July 1, 1994) requires us to solicit independent (4) Importing or exporting these Public Comments Solicited expert review from qualified specialists, species or any part of these species. To ensure that any final action concurrent with the public comment We emphasize that whether a resulting from this proposed rule will be period. The intent of the peer review violation results from a particular as accurate and effective as possible, we policy is to ensure that listings are based activity is entirely dependent upon the are soliciting comments and information on the best scientific and commercial facts and circumstances of each from the public, other concerned data available. We solicited peer review incident. Further, an activity not listed governmental agencies, the scientific comments on the species’ status review may in fact constitute a violation. community, industry, and any other reports (Casselbury and Carlson 2015a–

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g) from 22 scientists from the academic economic impacts cannot be considered List of Subjects and scientific community that were when assessing the status of a species. 50 CFR Part 223 either familiar with the species or had Therefore, the economic analysis expertise in elasmobranch biology, requirements of the Regulatory Endangered and threatened species, ecology, or conservation. We received Flexibility Act are not applicable to the Exports, Imports, Transportation. comments from nine scientists and listing process. In addition, this incorporated those comments into the proposed rule is exempt from review 50 CFR Part 224 status review reports and this proposed under Executive Order 12866. This Endangered and threatened species, rule. Their comments on the status proposed rule does not contain a reviews are also summarized in the peer Exports, Imports, Transportation. collection-of-information requirement review report available at http:// Dated: November 30, 2015. for the purposes of the Paperwork www.cio.noaa.gov/services_programs/ Reduction Act. Samuel D. Rauch, III, prplans/PRsummaries.html. Deputy Assistant Administrator for References Executive Order 13132, Federalism Regulatory Programs, National Marine Fisheries Service. A complete list of the references used In accordance with E.O. 13132, we in this proposed rule is available upon determined that this proposed rule does For the reasons set out in the request (see ADDRESSES). not have significant Federalism effects preamble, 50 CFR parts 223 and 224 are Classification and that a Federalism assessment is not proposed to be amended as follows: required. In keeping with the intent of National Environmental Policy Act the Administration and Congress to PART 223—THREATENED MARINE AND ANADROMOUS SPECIES The 1982 amendments to the ESA, in provide continuing and meaningful section 4(b)(1)(A), restrict the dialogue on issues of mutual state and ■ information that may be considered Federal interest, this proposed rule will 1. The authority citation for part 223 when assessing species for listing. Based be given to the relevant governmental continues to read as follows: on this limitation of criteria for a listing agencies in the countries in which the Authority: 16 U.S.C. 1531–1543; subpart decision and the opinion in Pacific species occurs, and they will be invited B, § 223.201–202 also issued under 16 U.S.C. Legal Foundation v. Andrus, 675 F. 2d to comment. We will confer with the 1361 et seq.; 16 U.S.C. 5503(d) for 825 (6th Cir. 1981), we have concluded U.S. Department of State to ensure § 223.206(d)(9). that ESA listing actions are not subject appropriate notice is given to foreign to the environmental assessment ■ 2. In § 223.102, amend the table in nations within the range of all three requirements of the National paragraph (e) by adding new entries for species. As the process continues, we Environmental Policy Act (NEPA) (See two species in alphabetical order under NOAA Administrative Order 216–6). intend to continue engaging in informal the ‘‘Fishes’’ table subheading to read as and formal contacts with the U.S. State follows: Executive Order 12866, Regulatory Department, giving careful Flexibility Act, and Paperwork consideration to all written and oral § 223.102 Enumeration of threatened marine and anadromous species. Reduction Act comments received. As noted in the Conference Report on * * * * * the 1982 amendments to the ESA, (e) * * *

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

*******

Fishes

******* Shark, spiny angel ...... Squatina guggenheim ...... Entire species ...... Federal Register citation NA NA and date when pub- lished as a final rule. Shark, narrownose Mustelus schmitti ...... Entire species ...... Federal Register citation NA NA smoothhound. and date when pub- lished as a final rule.

******* 1 Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement, see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56 FR 58612, November 20, 1991). 2 Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, is limited to turtles while in the water. [79 FR 20806, Apr. 14, 2014, as amended at 79 FR 38240, July 3, 2014; 79 FR 40015, July 11, 2014; 79 FR 54122, Sept. 10, 2014; 80 FR 7978, Feb. 13, 2015]

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

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

*******

Fishes

******* Guitarfish, Brazilian ...... Rhinobatos horkelii ...... Entire species ...... Federal Register citation NA NA and date when pub- lished as a final rule. Shark, Argentine angel ...... Squatina argentina ...... Entire species ...... Federal Register citation NA NA and date when pub- lished as a final rule. Shark, daggernose ...... Isogomphodon Entire species ...... Federal Register citation NA NA oxyrhynchus. and date when pub- lished as a final rule. Shark, striped Mustelus fasciatus ...... Entire species ...... Federal Register citation NA NA smoothhound. and date when pub- lished as a final rule.

******* 1 Species includes taxonomic species, subspecies, distinct population segments (DPSs) (for a policy statement, see 61 FR 4722, February 7, 1996), and evolutionarily significant units (ESUs) (for a policy statement, see 56 FR 58612, November 20, 1991). 2 Jurisdiction for sea turtles by the Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service, is limited to turtles while in the water. [79 FR 20814, Apr. 14, 2014, as amended at 79 FR 31227, June 2, 2014; 79 FR 38241, July 3, 2014; 79 FR 74005, Dec. 12, 2014; 79 FR 78725, Dec. 31, 2014; 79 FR 68372, Nov. 17, 2014; 80 FR 7978, Feb. 13, 2015; 80 FR 7390, Feb. 10, 2015]

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

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