Biology of Skates Developments in Environmental Biology of Fishes 27

Series Editor DAVID L.G. NOAKES

For further volumes: http://www.springer.com/series/5826 David A. Ebert · James A. Sulikowski Editors

Biology of Skates

123 Editors: David A. Ebert James A. Sulikowski Moss Landing Marine Laboratories University of New England Pacific Shark Research Center Marine Science Center Moss Landing, CA 95039, USA 11 Hills Beach Rd. Biddeford ME 04005, USA [email protected]

ISBN: 978-1-4020-9702-7 e-ISBN: 978-1-4020-9703-4

DOI: 10.1007/978-1-4020-9703-4

Library of Congress Control Number: 2008942792

© Springer Science+Business Media B.V. 2008

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Preface: Biology of skates by D.A. Ebert & J.A. Sulikowski ...... 1–4 Biodiversity and systematics of skates (Chondrichthyes: Rajiformes: Rajoidei) by D.A. Ebert & L.J.V. Compagno ...... 5–18 Southern African skate biodiversity and distribution by L.J.V. Compagno & D.A. Ebert ...... 19–39 Food habits of the sandpaper skate, Bathyraja kincaidii (Garman, 1908) off central California: seasonal variation in diet linked to oceanographic conditions by C.S. Rinewalt, D.A. Ebert & G.M. Cailliet ...... 41–57 Food habits of the longnose skate, Raja rhina (Jordan and Gilbert, 1880), in central California waters by H.J. Robinson, G.M. Cailliet & D.A. Ebert ...... 59–73 Dietary comparisons of six skate species (Rajidae) in south-eastern Australian waters by M.A. Treloar, L.J.B. Laurenson & J.D. Stevens . . . 75–90 Comparative feeding ecology of four sympatric skate species off central California, USA by J.J. Bizzarro, H.J. Robinson, C.S. Rinewalt & D.A. Ebert ...... 91–114 Standardized diet compositions and trophic levels of skates (Chondrichthyes: Rajiformes: Rajoidei) by D.A. Ebert & J.J. Bizzarro . . 115–131 Normal embryonic development in the clearnose skate, Raja eglanteria, with experimental observations on artificial insemination by C.A. Luer, C.J. Walsh, A.B. Bodine & J.T. Wyffels ...... 133–149 Endocrinological investigation into the reproductive cycles of two sympatric skate species, Malacoraja senta and Amblyraja radiata, in the western Gulf of Maine by J. Kneebone, D.E. Ferguson, J.A. Sulikowski & P.C.W. Tsang ...... 151–159 Morphological variation in the electric organ of the little skate (Leucoraja erinacea) and its possible role in communication during courtship by J.M. Morson & J.F. Morrissey ...... 161–169 Reproductive biology of Rioraja agassizi from the coastal southwestern Atlantic ecosystem between northern Uruguay (34°S) and northern Argentina (42°S) by J.H. Colonello, M.L. García & C.A. Lasta . . . . 171–178 Profiling plasma steroid hormones: a non-lethal approach for the study of skate reproductive biology and its potential use in conservation management by J.A. Sulikowski, W.B. Driggers III, G.W. Ingram Jr., J. Kneebone, D.E. Ferguson & P.C.W. Tsang ...... 179–186 Age and growth estimates for the smooth skate, Malacoraja senta, in the Gulf of Maine by L.J. Natanson, J.A. Sulikowski, J.R. Kneebone & P.C. Tsang ...... 187–202 Age, growth, maturity, and mortality of the Alaska skate, Bathyraja parmifera, in the eastern Bering Sea by M.E. Matta & D.R. Gunderson ...... 203–217 Age and growth of the roughtail skate Bathyraja trachura (Gilbert 1892) from the eastern North Pacific by C.D. Davis, G.M. Cailliet & D.A. Ebert ...... 219–230 Age and growth of big skate (Raja binoculata) and longnose skate (R. rhina) in the Gulf of Alaska by C.M. Gburski, S.K. Gaichas & D.K. Kimura ...... 231–243 Preface: Biology of skates

David A. Ebert Æ James A. Sulikowski

Originally published in the journal Environmental Biology of Fishes, Volume 80, Nos 2–3, 107–110. DOI 10.1007/s10641-007-9244-3 Ó Springer Science+Business Media B.V. 2007

Synopsis Skates have become a concern in growth. To the best of our knowledge this is the recent years due to the preponderance of these first dedicated book on the biology of skates. We elasmobranchs that are caught as bycatch or as a hope that readers will find this issue of interest directed fishery. This has raised concern because and that it helps encourage and stimulate future skates have life history characteristics that may research into these fascinating fishes. make them vulnerable to over-exploitation. It was due to this increasing awareness and concern Keywords Rajidae Á Symposium Á Life history about these batoids that prompted us to organize an international symposium on the ‘‘Biology of Skates have become a concern in recent years due Skates’’. The aims and goals of the symposium to the preponderance of these elasmobranchs to were to bring together an international group of be landed as part of a directed fishery or researchers to meet, discuss, perhaps develop indirectly as bycatch. This has raised concern collaborations, and present their most recent because skates, like other chondrichthyans, have findings. The symposium was held over two days, life history characteristics that make them vul- on 13–14 July, 2006, in conjunction with the 22nd nerable to over-exploitation. However, until annual meeting of the American Elasmobranch recently this ubiquitous batoid group has received Society in New Orleans, LA. A total of 31 authors little study relative to the charismatic shark-like from four countries contributed 16 papers that fishes that are the target of major fisheries appear in this special issue. The papers are worldwide. Furthermore, due to their demersal broadly arranged into four separate categories: life-style on soft bottom substrates skates are systematics and biogeography, diet and feeding especially vulnerable to trawl fisheries. Although, ecology, reproductive biology, and age and shark fisheries are now being scrutinized and managed more closely than ever, skates despite being one of the more common and visible & D. A. Ebert ( ) components of bycatch fisheries are generally still Pacific Shark Research Center, Moss Landing Marine Laboratories, 8272 Moss Landing Road, Moss overlooked. In Alaskan waters, for example, the Landing, CA 95039, USA biomass of skate discard has been estimated at e-mail: [email protected] over 25 million metric tons, while skate landings along the California coast have increased 10-fold J. A. Sulikowski Marine Science Center, University of New England, in the past 2 decades. It has been well 11 Hills Beach Road, Biddeford, ME 04005, USA documented that trawl fisheries in the North

D.A. Ebert & J.A. Sulikowski (eds.), Biology of Skates. DOI: 10.1007/978-1-4020-9703-4_1 1 2 D.A. Ebert & J.A. Sulikowski (eds.)

Atlantic have impacted the abundance, popula- meeting of the American Elasmobranch Society tion structure, and distribution of several skate in New Orleans, LA (Fig. 1). A total of 25 species, causing several to be given commercially speakers, representing nine countries, presented prohibited status. Given the increased awareness papers during the symposium proper with another and concern globally, researchers have begun to three papers and five posters presented during the pay closer attention to these enigmatic fishes and general and posters sessions, respectively. The have begun to study their biology with a new- presenters included a nice mix of established found sense of urgency. professionals (n = 12) and young budding It was due this increasing awareness and researchers (n = 13), about 10 of whom were concern about these fishes that prompted us to presenting results from their masters theses or organize an international symposium on the Ph.D. dissertations. ‘‘Biology of Skates’’. The aims and goals of the A total of 31 authors from four countries symposium were to bring together an interna- contributed 16 papers that appear in this special tional group of researchers to meet, discuss, issue. The papers are broadly arranged into the perhaps develop collaborations, and present their same four separate categories as the symposium: most recent findings. The symposium was broadly systematics and biogeography, diet and feeding organized around four areas of research, system- ecology, reproductive biology, and age and atics and biogeography, diet and feeding ecology, growth. The first paper by David Ebert and reproductive biology, and age and growth aspects Leonard Compagno presents a historical perspec- of their biology. Our initial inquiry to gauge the tive on skate systematics over the past 250 years, interest of such a symposium was very well chronologically detailing the exponential growth received as approximately 75 researchers from in skate diversity, e.g. number of species and nearly 20 countries responded positively. The genera, and how a few individual researchers over overwhelming response we received confirmed the past 60 years have largely been responsible our belief that there was a high level of interest, for this dynamic increase in skate numbers. and concern, for skates. Included in this paper, in an appendix, is a The symposium was held over 2 days, on 13–14 checklist of all living skate species. Leonard July 2006, in conjunction with the 22nd annual Compagno and David Ebert then present a

Fig. 1 Participants at the Biology of Skates symposium cis, Carl Luer, Joe Bizzarro, Michelle Treloar, Dana held in conjunction with the 22nd Annual American Bethea, David Ebert, Beth Matta, James Sulikowski, Chris Elasmobranch Society meeting in New Orleans, 13–14 Gburski, Duane Stevenson, Jim Ellis, Jorge Colonello, July, 2006. From left to right; Jeff Kneebone, Romney Daniel Figueroa, Dave Kulka, Jason Morson. Absent from McPhie, Chante´ Davis, Lisa Natanson, Chris Rinewalt, photograph: Marcelo de Carvalho, Peter Last, and John Oscar Sosa Nishizaki, Heather Robinson, Malcolm Fran- McEachran Biology of Skates 3 regional account on the biodiversity of skates alternative to study reproductive biology in male from their nearly 25 years of research on the and female skates. The final portion of this special southern African fauna. In his paper on the issue presents four excellent studies detailing the feeding ecology of the sandpaper skate, Bathyraja age and growth of five skate species. The first kincaidii, Christopher Rinewalt and co-authors paper by Lisa Natanson and her co-authors demonstrate by use of a three-factor MANOVA presents age and growth estimates for the smooth significant differences in the diet of this skate by skate, Malacoraja senta, in the Gulf of Maine sex, maturity status, and oceanographic season using an innovative histological technique to using numeric and gravimetric measures of enhance band clarity. This is followed by two importance for the major prey categories. papers presenting the first age and growth esti- Heather Robinson and her co-authors report on mates for two North Pacific Ocean skate species. a dietary shift from crustaceans to teleosts asso- Beth Matta and Donald Gunderson in their paper ciated with depth and size in the longnose skate, on aspects of the age, growth, maturity, and Raja rhina, a moderately large eastern North mortality of the Alaska skate, Bathyraja parmif- Pacific species. The following two papers, by era, found that caudal thorns may represent a Michelle Treloar and Joe Bizzarro and their non-lethal method to estimate age and growth in collaborators, each deal with the trophic ecology this species. Conversely, Chante Davis and her of a complex of skates from southeastern Aus- co-authors in their study on the age and growth of tralia and central California, USA, respectively. the roughtail skate, Bathyraja trachura, a com- The final paper on diet and feeding ecology is by mon mid to upper slope species, found that caudal David Ebert and Joe Bizzarro, and examines the thorns were not a useful method for estimating standardized diet composition and trophic levels age in this species. These two studies illustrate the of skates, finding that these fish occupy a similar importance of analyzing and interpreting ageing tophic position to that of other upper trophic structures, e.g. vertebrae and caudal thorns, on an level marine predators. The five papers on skate individual species basis. This special issue con- reproductive biology cover a wide range of cludes with an important paper by Christopher aspects, including one by Carl Luer and col- Gburski and his collaborators on the age and leagues on embryonic development of the clear- growth of two skates (Raja binoculata and R. nose skate, Raja eglanteria, with observations on rhina) that have been at the center of an emerging artificial insemination in this species, a technique fishery in the Gulf of Alaska. Results from this which may have important implications on other study will be critical to developing demographic captive elasmobranchs. Jeff Kneebone and his co- models for stock assessments in these two species. authors investigated the seasonal cycle of two To the best of our knowledge this is the first common Gulf of Maine skates by examining dedicated book on the biology of skates. We hope seasonal changes in steroid hormone levels over that the readers find this issue of interest and that the course of a year. Jason Morson and John it helps encourage and stimulate future research Morrissey demonstrate that the electric organ into these fascinating fishes. discharge in little skates, Leucoraja erinacea, may We as guest editors would like to thank all of play a role in communication during courtship. the participants who presented papers and posters Jorge Colonello and his colleagues examined the at the symposium and to Environmental Biology seasonal reproductive cycle of the monotypic Rio of Fishes (EBF) for publishing this special issue, skate, Rioraja agassiz, a common southwestern especially the editor in chief, David Noakes, Atlantic species of the continental shelf, conclud- managing editor, Lynn Bouvier, and the staff at ing that females have a partially defined repro- EBF for making this a smooth process. Funding ductive cycle with two peaks seasons. James for the ‘‘Biology of Skates’’ Symposium was Sulikowski and collaborators conclude the repro- provided by NOAA/NMFS to the National Shark ductive part of this issue by presenting evidence Research Consortium and Pacific Shark Research that circulating levels of estradiol and testoster- Center and by the American Elasmobranch one concentrations can be used as a non-lethal Society. Finally, we would like to thank the 4 D.A. Ebert & J.A. Sulikowski (eds.) following referees for taking the time out of their Referees Institution busy schedules to expeditiously review manu- scripts, in a timely manner, for this special issue. Mabel Manjaji- University Malaysia Sabah, Malaysia (*Number in parenthesis indicates more than one Matsumoto Beth Matta NOAA Fisheries Service, Alaska manuscript reviewed). Fisheries Science Center Romney McPhie Dalhousie University, Canada Lisa Natanson NOAA Fisheries Service, Northeast Fisheries Science Center Christopher Moss Landing Marine Laboratories, Referees Institution Rinewalt Pacific Shark Research Center Heather Moss Landing Marine Laboratories, Cynthia Awruch University of Tasmania, Australia Robinson Pacific Shark Research Center Ivy Baremore NOAA Fisheries Services, Southeast Duane Stevenson NOAA Fisheries Service, Alaska Fisheries Science Center Fisheries Science Center Lewis Barnett Moss Landing Marine Laboratories, Adam Summers Ecology and Evolutionary Biology, Pacific Shark Research Center University California Irvine Dana Bethea NOAA Fisheries Service, Southeast Michelle Treloar CSIRO Marine Research, Australia Fisheries Science Center (2) Joseph Bizzarro Moss Landing Marine Laboratories, Paul Tsang University of New Hampshire (2) Pacific Shark Research Center William White CSIRO Marine Research, Australia Juan Matias University of Adelaide, Australia (2) Braccini Gregor Cailliet Moss Landing Marine Laboratories, Pacific Shark Research Center Enric Corte´s NOAA Fisheries Service, Southeast Fisheries Science Center Paul Cowley South African Institute of Aquatic Biodiversity, South Africa Chante´ Davis Moss Landing Marine Laboratories, Pacific Shark Research Center Marcelo de University of Sa˜o Paulo, Brazil Carvalho Jim Ellis CEFAS, Lowestoft Laboratory, England Lara Ferry- Moss Landing Marine Laboratories Graham Malcolm Francis National Institute of Water and Atmospheric Research, New Zealand Christopher National Marine Fisheries Service, Gburski Alaska Fisheries Science Center Jim Gelsleichter Mote Marine Laboratory Kenneth Alaska Department of Fish & Game Goldman Dean Grubbs Virginia Institute of Marine Science, College of William & Mary Alan Henningsen National Aquarium in Baltimore Gerald Hoff NOAA Fisheries Service, Alaska Fisheries Science Center Brett Human Marine Science and Fisheries Centre of Oman Sarah Irvine Deakin University, Australia Hajime Ishihara Taiyo Engineering Overseas, Japan Jeff Kneebone University of New Hampshire David Koester University of New England David Kulka Department of Fisheries & Oceans, Canada Luis Lucifora Dalhousie University, Canada Biodiversity and systematics of skates (Chondrichthyes: Rajiformes: Rajoidei)

David A. Ebert Æ Leonard J. V. Compagno

Originally published in the journal Environmental Biology of Fishes, Volume 80, Nos 2–3, 111–124. DOI 10.1007/s10641-007-9247-0 Ó Springer Science+Business Media B.V. 2007

Abstract Skates (Rajiformes: Rajoidei) are a highly uted to a better understanding of the diversity of the diverse fish group, comprising more valid species skates. A checklist of the living valid skate species is than any other group of cartilaginous fishes. The high presented. degree of endemism exhibited by the skates is somewhat enigmatic given their relatively conserved Keywords Skates Á Classification Á Arhychobatidae Á body morphology and apparent restrictive habitat, Anacanthobatidae Á Rajidae Á Checklist e.g. soft bottom substrates. Skates are primarily marine benthic dwellers found from the intertidal down to depths in excess of 3,000 m. They are most Introduction diverse at higher latitudes and in deepwater, but are replaced in shallower, warm temperate to tropical Batoids (Chondrichthyes: Rajiformes), including the waters by stingrays (Myliobatodei). The number of skates (suborder: Rajoidei), comprises more valid valid skate species has increased exponentially, with species (n = 574) than all of the other nine more species having been described since 1950 chondrichthyan orders combined (n = 528) (Fig. 1). (n = 126) than had been described in the previous They comprise more than twice the number of 200 years (n = 119). Much of the renaissance in skate chondrichthyan species relative to the nearest group, systematics has largely been through the efforts of a the Carcharhiniformes (n = 296). Furthermore, few individuals who through author–coauthor collab- among batoids, the skates (Rajoidei) are the most oration have accounted for 78 of the 131 species diverse group comprising more genera (n = 27) and described since 1948 and for nine of 13 genera named species (n = 245) than any of the other nine batoid since 1950. Furthermore, detailed regional surveys suborders (Fig. 2). The stingrays (Myliobatoidei), the and accounts of skate biodiversity have also contrib- other most diverse batoid suborder, are morpho- gically far more varied than skates and show a far richer diversity at the family level (n = 10) and nearly & D. A. Ebert ( ) as many genera (n = 24). Overall, the total number of Pacific Shark Research Center, Moss Landing Marine Laboratories, skate species represents over 22% of all known Moss Landing, CA 95039, USA chondrichthyan species and about 43% of all batoids. e-mail: [email protected] The high degree of biodiversity and endemism exhibited by skates is somewhat enigmatic given L. J. V. Compagno Shark Research Center, Iziko – Museums of Cape Town, their relatively conservative dorso-ventrally flattened Cape Town 8000, South Africa body morphology and apparent restrictive habitat

D.A. Ebert & J.A. Sulikowski (eds.), Biology of Skates. DOI: 10.1007/978-1-4020-9703-4_2 5 6 D.A. Ebert & J.A. Sulikowski (eds.)

Fig. 1 The number of Chimaeriformes (chimaeras) described valid Chondrichthyan species per Carcharhiniformes (ground sharks) order as compiled by the authors as of 2 March 2007. Lamniformes (mackerel sharks) Solid bar is number of Orectolobiformes (carpet sharks) batoid species excluding skates and open bar s Heterodontiformes (horn sharks) r e represents number of skate d r species O Squatiniformes (angel sharks)

Pristiophoriformes (sawsharks)

Squaliformes (dogfish sharks)

Hexanchiformes (cow & frilled sharks)

Rajiformes (batoids) 0 100 200 300 400 500 600 700 Number of species

Fig. 2 The total number of families, genera, and Pristoidei (Sawfishes) species per batoid suborder Family Rhinoidei (Sharkrays) as compiled by the authors Genera as of 2 March 2007. The Species suborders Rhinoidei, Rhynchobatoidei (Wedgefishes) s

Rhynchbatoidei, r e Rhinobatoidei (Guitarfishes) d

Rhinobatoidei, and r o

Zanobatoidei each have b u Platyrhinoidei (Thornback and Fanrays) s only a single family and d i

genus, while the suborders o t Zanobatoidei (Panrays) Pristoidei and a B Platyrhinoidei each have a Torpedinoidei (Electric rays) monotypic family and two genera each Myliobatoidei (Stingrays)

Rajoidei (Skates)

0 50 100 150 200 250 300 Relative total numbers preference, e.g. soft bottom substrates. Skates are be primarily inhabitants of soft bottom substrates, primarily marine benthic dwellers found from the recent research by remote operated vehicles has intertidal down to depths in excess of 3,000 m. Skates revealed a somewhat diverse skate fauna inhabiting are most diverse at higher latitudes and in deeper areas of rock cobble to high rocky relief. Several waters, but are generally replaced in shallower, eastern North Pacific species once considered uncom- warmer, temperate to tropical waters by Mylioba- mon are in fact quite common in areas previously toids. Skates are generally found in shallower waters considered uninhabitable for skates (Kuhnz et al. towards the poles, but occur deeper in warm temper- 2006). ate to tropical equatorial waters. They are conspic- The number of valid skate species has increased uously absent from brackish and freshwater environs, exponentially over the past century (Fig. 3). Prior to except for a single estuarine species found in 1900 only 62 skate species had been described, with Tasmania, Australia (species ‘‘L’’ in Last and another 57 species being described between 1900 and Stevens 1994) and there are no known pelagic 1949 that brought the total number to 119 described species within this group. Although long thought to species. However, since 1950 126 skate species have Biology of Skates 7

Fig. 3 Number of skate 2000 to 2006 species described by decade 1990 to 1999 from 1750 to 2006. Number 1980 to 1989 of valid species compiled 1970 to 1979 by authors as of 2 March 1960 to 1969 2007 1950 to 1959 1940 to 1949 1930 to 1939 1920 to 1929 1910 to 1919 e

d 1900 to 1909 a c

e 1890 to 1899 D 1880 to 1889 1870 to 1879 1860 to 1869 1850 to 1859 1840 to 1849 1830 to 1839 1820 to 1829 1810 to 1819 1800 to 1809 1750 to 1759 0 5 10 15 20 25 30 35 Number of skate species been described. This rapid increase over the past Hulley (n = 5), Carolus Linnaeus (n = 5), Johannes nearly 60 years was due largely to the efforts of five Mu¨ller and Fredrich Gustav Jacob Henle (n = 5), individuals who through author–coauthor combina- Cecil von Bonde and D.B. Swart (n = 5), and John tions have accounted for 78 (59.5%) of the 131 Wallace (n = 5). species described since 1948. At the forefront of this Paralleling the increase in skate species has been renaissance in skate systematics was the collaboration an increase in the number of recognized genera of Henry Bigelow and William Schroeder who (Fig. 4). Of the 27 recognized skate genera, 21 have accounted for the most new species descriptions with beenerectedsince1900with13havingbeen 29 (Bigelow and Schroeder 1948, 1950, 1951a, b, described since 1950 alone. As with the increase in 1954, 1958, 1962, 1964, 1965). Also, contributing new species descriptions there have been a few during the 1950’s and 60’s was Ishiyama (1952, individuals who through author–coauthor combina- 1955, 1958, 1967) who named 10 species and later in tions have been responsible for naming most of the collaboration with his student Hajime Ishihara, who skate genera. Ishiyama (1952, 1958) has authored the has contributed much to the systematics of skates in most with four (Bathyraja, Notoraja, Okamejei, his own right, described another five species (Ishiy- Rhinoraja) generic descriptions, followed by Gilbert ama and Ishihara 1977; Ishihara and Ishiyama 1985). Whitley who described three (Whitley 1931, 1939; Since the early 1970’s two individuals, John Irolita, Pavoraja, Rioraja), and Bigelow and Schroe- McEachran and Mathias Stehmann, have each either der (1948, 1954) who collaborated in naming three authored or coauthored the descriptions of 18 and 16 (Breviraja, Cruriraja, Pseudoraja) genera. McEach- species each, respectively. Other notable ichthyolo- ran in collaboration with Leonard Compagno and gists who have been involved in authoring–coauthor- Peter Last has also contributed to the descriptions of ing the descriptions of five or more skate species three (Brochiraja, Fenestraja, Neoraja) skate genera. includes (with number of species), V.N. Dolganov Those having authored–coauthored the descriptions (n = 7), Samuel Garman (n = 7), David Starr Jordan of two genera include Compagno (McEachran and (n = 7), John Norman (n = 7), Hajime Ishihara Compagno 1982), Stehmann (1970; Malacoraja, (n = 6), Peter Last (n = 6), Charles Gilbert (n = 6), Rajella), and A. W. Malm (Malm (1877; Amblyraja, Albert Gu¨nther (n = 6), P. Alexander ‘‘Butch’’ Leucoraja).