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Squaliformes: Centrophoridae: Centrophorus) in North Atlantic Waters - Current Status and Taxonomic Issues

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Squaliformes: Centrophoridae: Centrophorus) in North Atlantic Waters - Current Status and Taxonomic Issues W&M ScholarWorks VIMS Articles Virginia Institute of Marine Science 2014 Species diversity of the deep-water gulper sharks (Squaliformes: Centrophoridae: Centrophorus) in North Atlantic waters - current status and taxonomic issues A Verissimo Virginia Institute of Marine Science CF Cotton Virginia Institute of Marine Science RH Buch J Guallart GH Burgess Follow this and additional works at: https://scholarworks.wm.edu/vimsarticles Part of the Aquaculture and Fisheries Commons Recommended Citation Verissimo, A; Cotton, CF; Buch, RH; Guallart, J; and Burgess, GH, Species diversity of the deep-water gulper sharks (Squaliformes: Centrophoridae: Centrophorus) in North Atlantic waters - current status and taxonomic issues (2014). Zoological Journal Of The Linnean Society, 172(4), 803-830. 10.1111/zoj.12194 This Article is brought to you for free and open access by the Virginia Institute of Marine Science at W&M ScholarWorks. It has been accepted for inclusion in VIMS Articles by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. bs_bs_banner Zoological Journal of the Linnean Society, 2014, 172, 803–830. With 12 figures Downloaded from https://academic.oup.com/zoolinnean/article-abstract/172/4/803/2433424 by VIRGINIA INSTITUTE OF Marine Science user on 30 October 2018 Species diversity of the deep-water gulper sharks (Squaliformes: Centrophoridae: Centrophorus) in North Atlantic waters – current status and taxonomic issues ANA VERÍSSIMO1,2*, CHARLES F. COTTON2,3,4, ROBERT H. BUCH5,6, JAVIER GUALLART7 and GEORGE H. BURGESS5 1CIBIO-UP – Center for Research in Biodiversity and Genetic Resources, Rua Padre Armando Quintas, Campus Agrário de Vairão, 4485-661 Vairão, Portugal 2Department of Fisheries Science, Virginia Institute of Marine Science, College of William and Mary, P.O. Box 1346, Gloucester Point, VA 23062, USA 3Department of Marine and Environmental Sciences, Savannah State University, 3219 College Street, Box 20467, Savannah, GA 31404, USA 4Florida State University Coastal and Marine Lab, 3618 Highway 98, St. Teresa, FL 32358, USA 5Florida Program for Shark Research, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611, USA 6NOAA Fisheries Service, Northeast Regional Office (NERO), Gloucester, MA 01930, USA 7Laboratorio de Biología Marina, Departamento de Zoología, Universitat de València. E-46100 Burjassot (Valencia), Spain Received 18 December 2013; revised 15 July 2014; accepted for publication 28 July 2014 The gulper sharks (genus Centrophorus) are a group of deep-water benthopelagic sharks with a worldwide dis- tribution. The alpha taxonomy of the group has historically been problematic and the number of species included in the genus has varied considerably over the years and is still under debate. Gulper sharks are routinely caught in mid- and deep-water fisheries worldwide and some have shown a considerable decline in abundance in the last few decades. Clear and consistent species discrimination of Centrophorus is essential for an efficient and sustain- able management of these fisheries resources. Our study used molecular cytochrome oxidase subunit I (COI) and 16S ribosomal RNA gene sequences and morphometric data to re-evaluate the diversity of Centrophorus in North Atlantic waters, including the Gulf of Mexico, the Caribbean, and the Mediterranean Seas. Molecular data sepa- rated North Atlantic Centrophorus into five well-supported groups whereas morphometric data separated these same five groups and suggested three additional groups for which no molecular data were available. Four of the five groups identified in the North Atlantic also occur in the Indian and/or Pacific Oceans, thus extending the reported range of some species considerably. A species identification key for North Atlantic Centrophorus is pro- vided based on our findings. © 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 172, 803–830. doi: 10.1111/zoj.12194 ADDITIONAL KEYWORDS: alpha taxonomy – dichotomous key – dogfishes – molecular genetics – morphometrics – squaloid. INTRODUCTION of small- to medium-sized species (< 200 cm total length, TL) commonly known as gulper sharks. These are The genus Centrophorus Müller & Henle, 1837 (order benthopelagic sharks often found along the outer con- Squaliformes: family Centrophoridae) comprises a group tinental shelves and upper continental and insular slopes at depths between 50 and 2350 m throughout the world’s *Corresponding author. E-mail: [email protected] oceans (Compagno, 1984; McEachran & Branstetter, © 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 172, 803–830 803 804 A. VERÍSSIMO ET AL. 1984). The first description of a gulper shark dates back original species types and problematic specimens cannot to the late 18th century, i.e. Centrophorus (Squalus) be made or are of limited usefulness because precise squamosus (Bonnaterre, 1788), although the genus morphometric data are almost impossible to obtain from Downloaded from https://academic.oup.com/zoolinnean/article-abstract/172/4/803/2433424 by VIRGINIA INSTITUTE OF Marine Science user on 30 October 2018 Centrophorus was proposed only in the mid 19th century the type specimens. Another complicating factor stems by Müller & Henle (1837a, b). The genus was based from the unreliability of some diagnostic morphologi- on the description of Squalus granulosus by Bloch & cal characters previously used for species identifica- Schneider (1801), which then became the type species, tion. Some often-used diagnostic characters vary with i.e. Centrophorus granulosus (Müller & Henle, 1841). ontogeny, such as shape and size of pectoral fin inner Since then, over 30 nominal species have been re- margins, and shape of dermal denticles, teeth, or of ferred to the genus Centrophorus (Eschmeyer, 2013) dorsal spines (Cadenat, 1959a, c; Maurin, 1968; Bass although some of them were subsequently assigned to et al., 1976; Ledoux, 1970; Cadenat & Blache, 1981; other genera (e.g. Centroscymnus Bocage & Capello, Tabit, 1993; Guallart, 1998; Guallart, García-Salinas 1864 or Deania Jordan & Snyder, 1902). & Catalán, 2013; White et al., 2013). As a result, dis- Although some of the species were described more tinct ontogenetic stages of the same species (ju- than two centuries ago, the global diversity of gulper veniles vs. adults) have been considered as distinct taxa sharks is not yet fully described (Castro, 2011; Naylor (e.g. White et al., 2013 determined Centrophorus acus et al., 2012; present study). Many authors have made Garman, 1906, described from a juvenile, to be a junior regional or global revisions of Centrophorus alpha tax- synonym of C. granulosus). onomy over the last 50 years, but they have also noted Ambiguous and inconsistent species identification plus the provisional character of their conclusions (Bigelow the continued debate amongst some systematists over & Schroeder, 1957; Bass, D’Aubrey & Kistnasamy, 1976; few, cosmopolitan species vs. multiple, less wide- Cadenat & Blache, 1981; Compagno, 1984; McEachran ranging species have generated much confusion in the & Branstetter, 1984; Bass, Compagno & Heemstra, 1986; literature, and a worldwide revision of the genus Last & Stevens, 1994). Other authors have described Centrophorus is much needed. This is particularly rel- previously unidentified morphotypes or have suggest- evant for certain species of gulper sharks that are com- ed the necessity to describe some new species (Cadenat monly targeted or bycaught in deep-water fisheries. & Blache, 1981; Castro, 2011; Naylor et al., 2012; present Studies have already shown signs of localized deple- study). As such, the number of species of Centrophorus tion for some Centrophorus species (Graham, Andrew is still not well defined (e.g. 13 recognized species in & Hodgson, 2001; ICES, 2006) and six species of Compagno, Dando & Fowler, 2005; 13 species in Ebert Centrophorus have been listed as Vulnerable, Near & Stehmann, 2012; 15 species in Eschmeyer, 2013). Threatened, or Endangered on the IUCN Red List Species discrimination within Centrophorus has been (iucnredlist.org accessed on 18 November 2013). Ad- problematic almost since its origin and still remains equate management and conservation efforts require problematic today. There are several issues contrib- reliable species-specific catch and mortality time series, uting to the confusion in the alpha taxonomy of as well as species-specific life history and ecological Centrophorus. One of the main problems is the high data. These data can be biased if species identifica- degree of morphological similarity between nominal taxa, tion is ambiguous or inconsistent, thus compromis- making species determination extremely challenging ing the effectiveness and adequacy of any management even for those experienced with the genus. Moreover, and conservation plan (Iglésias, Toulhoat & Sellos, 2010). many original species descriptions often fail to de- The eastern North Atlantic is one of the regions where scribe informative characters required to clearly dis- catches of deep-water sharks have been declining over tinguish nominal species from their congeners, a problem the past decades and total allowed catches (TAC) have that is particularly prevalent amongst the earliest de- been set to zero since 2010 for several species, includ- scribed taxa like in Centrophorus granulosus (Bloch ing C. granulosus and C. squamosus (ICES 2012). Un- & Schneider, 1801) and Centrophorus lusitanicus
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