Biology of Skates

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 Contents 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 ?rst dedicated book on the biology of skates. We elasmobranchs that are caught as bycatch or as a hope that readers will ?nd this issue of interest directed ?shery. This has raised concern because and that it helps encourage and stimulate future skates have life history characteristics that may research into these fascinating ?shes. make them vulnerable to over-exploitation. It was due to this increasing awareness and concern Keywords Rajidae Symposium 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 ?shery 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 ?ndings. 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 ?shes that are the target of major ?sheries 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 ?sheries. Although, ecology, reproductive biology, and age and shark ?sheries 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 ?sheries are generally still Paci?c 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: 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 ?ve posters presented during the pay closer attention to these enigmatic ?shes 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 ?shes 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 ?ndings. 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 ?rst 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 con?rmed 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 ?nal 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 ?ve skate species. The ?rst 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 signi?cant 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 ?rst age and growth esti- Heather Robinson and her co-authors report on mates for two North Paci?c 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- Paci?c 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 ?nal 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, ?nding that these ?sh 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 ?ve 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 arti?cial insemination in this species, a technique ?shery 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 ?rst 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 ?nd 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 ?shes. 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 de?ned 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 Paci?c 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 Matsumoto (*Number in parenthesis indicates more than one 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 Paci?c Shark Research Center Heather Moss Landing Marine Laboratories, Cynthia Awruch University of Tasmania, Australia Robinson Paci?c 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, Paci?c 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) Paci?c Shark Research Center William White CSIRO Marine Research, Australia Juan Matias University of Adelaide, Australia (2) Braccini Gregor Cailliet Moss Landing Marine Laboratories, Paci?c 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, Paci?c 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