Sharks of the Open Ocean

Sharks of the Open Ocean Biology, Fisheries and Conservation

Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

Fish and Aquatic Resources Series Series Editor: Tony J. Pitcher Director, Fisheries Centre, University of British Columbia, Canada The Blackwell Publishing Fish and Aquatic Resources Series is an initiative aimed at providing key books in this fast-moving field, published to a high international standard. The Series includes books that review major themes and issues in the science of fishes and the interdisciplinary study of their exploitation in human fisheries. Volumes in the Series combine a broad geographical scope with in-depth focus on concepts, research frontiers, and analytical frameworks. These books will be of interest to research workers in the biology, zoology, ichthyology, ecology, and physiology of fish and the economics, anthropology, sociology, and all aspects of fisheries. They will also appeal to non-specialists such as those with a commercial or industrial stake in fisheries. It is the aim of the editorial team that books in the Blackwell Publishing Fish and Aquatic Resources Series should adhere to the highest academic standards through being fully peer reviewed and edited by specialists in the field. The Series books are produced by Blackwell Publishing in a prestigious and distinctive format. The Series Editor, Professor Tony J. Pitcher, is an experienced international author, and founding editor of the leading journal in the field of fish and fisheries. The Series Editor and Publisher at Blackwell Publishing, Nigel Balmforth, will be pleased to discuss suggestions, advise on scope, and provide evaluations of proposals for books intended for the Series. Please see contact details listed below. Titles currently included in the Series (Full details at www.blackwellfish.com) 1. Effects of Fishing on Marine Ecosystems and Communities (S. Hall) 1999 2. Salmonid Fishes (Edited by Y. Altukhov et al.) 2000 3. Percid Fishes (J. Craig) 2000 4. Fisheries Oceanography (Edited by P. Harrison and T. Parsons) 2000 5. Sustainable Fishery Systems (A. Charles) 2000 6. Krill (Edited by I. Everson) 2000 7. Tropical Estuarine Fishes (S. Blaber) 2000 8. Recreational Fisheries (Edited by T. J. Pitcher and C. E. Hollingworth) 2002 9. Flatfishes (Edited by R. Gibson) 2005 10. Fisheries Acoustics (J. Simmonds and D. N. MacLennan) 2005 11. Fish Cognition and Behavior (Edited by C. Brown, K. Laland and J. Krause) 2006 12. Seamounts (Edited by T. J. Pitcher, T. Morato, P. J. B. Hart, M. R. Clark, N. Haggan and R. S. Santos) 2007 13. Sharks of the Open Ocean (Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock) 2008 For further information concerning books in the series, please contact: Nigel Balmforth, Professional Division, Blackwell Publishing, 9600 Garsington Road, Oxford OX4 2DQ, UK Tel:
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Sharks of the Open Ocean Biology, Fisheries and Conservation Edited by

Merry D. Camhi Conservation Consultant, USA

Ellen K. Pikitch Pew Institute for Ocean Science, Rosenstiel School of Marine and Atmospheric Science, University of Miami, USA

Elizabeth A. Babcock Pew Institute for Ocean Science, Rosenstiel School of Marine and Atmospheric Science, University of Miami, USA

Blackwell Science

© 2008 by Blackwell Publishing Ltd Blackwell Publishing editorial offices: Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK Tel:
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1 515 292 0140 Blackwell Publishing Asia Pty Ltd, 550 Swanston Street, Carlton, Victoria 3053, Australia Tel:
61 (0)3 8359 1011 The right of the Author to be identified as the Author of this Work has been asserted in accordance with the Copyright, Designs and Patents Act 1988. All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs and Patents Act 1988, without the prior permission of the publisher. Designations used by companies to distinguish their products are often claimed as trademarks. All brand names and product names used in this book are trade names, service marks, trademarks or registered trademarks of their respective owners. The Publisher is not associated with any product or vendor mentioned in this book. This publication is designed to provide accurate and authoritative information in regard to the subject matter covered. It is sold on the understanding that the Publisher is not engaged in rendering professional services. If professional advice or other expert assistance is required, the services of a competent professional should be sought. First published 2008 by Blackwell Publishing Ltd ISBN: 978 0632 05995 9 Library of Congress Cataloging-in-Publication Data Sharks of the open ocean : biology, fisheries and conservation / edited by Merry D. Camhi, Ellen K. Pikitch, Elizabeth A. Babcock. p. cm. — (Fish and aquatic resources series) ISBN-13: 978-0-632-05995-9 (hardback : alk. paper) ISBN-10: 0-632-05995-8 (harback : alk. paper) 1. Sharks. 2. Shark fisheries. 3. Sharks—Conservation. I. Camhi, Merry. II. Pikitch, Ellen K. III. Babcock, Elizabeth A. QL638.9.S487 2008 597.3—dc22 2007039627 A catalogue record for this title is available from the British Library Set in 10/13 pt Times by Charon Tec Ltd (A Macmillan Company), Chennai, India (www.charontec.com) Printed and bound in Singapore by Markono Print Media Pte Ltd The publisher’s policy is to use permanent paper from mills that operate a sustainable forestry policy, and which has been manufactured from pulp processed using acid-free and elementary chlorine-free practices. Furthermore, the publisher ensures that the text paper and cover board used have met acceptable environmental accreditation standards. For further information on Blackwell Publishing, visit our website: www.blackwellpublishing.com

Dedications

To my eternally supportive family: Zoe, Tasha and John, and the sharks of the open ocean – long may they roam. Merry D. Camhi To my family, including my parents, children, and husband, to my extended human family of relatives, friends, and colleagues, and to all living creatures on this blue planet, especially sharks. Ellen K. Pikitch To my mother and father. Elizabeth A. Babcock

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Contents

List of Contributors Series Foreword Foreword Acknowledgments Part I Introduction and Overview 1 Introduction to Sharks of the Open Ocean Ellen K. Pikitch, Merry D. Camhi and Elizabeth A. Babcock

2

3

xxi xxix xxxii xxxiv 1 3

Introduction The need for oceanic shark research and management Evaluating the conservation status of open ocean sharks The future of oceanic sharks References

3 4 6 8 10

Pelagic Elasmobranch Diversity Leonard J. V. Compagno

14

Introduction Pelagic shark diversity Pelagic sharks in perspective Acknowledgments References

14 15 20 22 22

The Reproductive Biology of Pelagic Elasmobranchs Franklin F. Snelson Jr., Brenda L. Roman and George H. Burgess

24

Introduction Methods and definitions Modes of reproduction Reproductive trends in pelagic elasmobranchs Reproduction in lamniform sharks Litter size Birth size Gestation period Reproductive periodicity

24 25 25 27 28 28 30 31 32

viii

Contents

Age and size at maturity Development Reproduction in requiem sharks Litter size Birth size Gestation period Reproductive periodicity Age and size at maturity Development Reproduction in the pelagic stingray Litter size Birth size Gestation period Reproductive periodicity Age and size at maturity Development Discussion References Part II

4

5

Life History and Status of Pelagic Elasmobranchs Introduction Biology and ecology Fisheries and status Conclusion

34 36 37 37 38 39 39 39 40 41 41 41 41 42 42 42 43 45 55 57 57 58 59

The Biology and Ecology of Thresher Sharks (Alopiidae) Susan E. Smith, Randall C. Rasmussen, Darlene A. Ramon and Gregor M. Cailliet

60

Introduction Distribution and movements Biology and ecology Age and growth Reproduction Diet Threats and status Acknowledgments References

60 60 62 62 64 64 65 66 66

The Biology and Ecology of the White Shark, Carcharodon carcharias Barry D. Bruce

69

Introduction Distribution, movements, and stock structure Geographic distribution Tagging studies and in situ observations

69 70 70 71

Contents

Seasonal movements Effects of temperature Stock structure Biology and ecology Age and growth Mortality Reproduction Diet Threats and status Acknowledgments References 6

7

8

Case Study: White Shark Movements in the North Pacific Pelagic Ecosystem Andre M. Boustany, Kevin C. M. Weng, Scot D. Anderson, Peter Pyle and Barbara A. Block

ix

71 71 72 72 72 74 74 75 75 76 76

82

Introduction Methods and Results References

82 83 85

The Biology and Ecology of the Shortfin Mako Shark, Isurus oxyrinchus John D. Stevens

87

Introduction Biology and ecology Age and growth Reproduction Diet Distribution and movements Distribution Migration and movements Threats and status Fisheries Stock structure and status References

87 88 88 89 89 89 89 89 90 90 91 91

The Biology and Ecology of the Salmon Shark, Lamna ditropis Kenneth J. Goldman and John A. Musick

95

Introduction Biology and ecology Distribution and movements Threats and status

95 96 98 100

x

9

10

11

Contents

Acknowledgments References

101 102

The Biology and Ecology of the Porbeagle Shark, Lamna nasus Malcolm P. Francis, Lisa J. Natanson and Steven E. Campana

105

Introduction Distribution, movements, and stock structure Biology and ecology Length–length and length–weight relationships Length at birth and maturity Growth, maturity, and recruitment Maximum length, longevity, and natural mortality Length, age, and sex composition Reproduction Diet Threats and status Fisheries Stock status Acknowledgments References

105 106 107 107 107 107 109 109 110 110 110 110 111 111 111

The Biology and Ecology of the Silky Shark, Carcharhinus falciformis Ramón Bonfil

114

Introduction Distribution, movements, and stock structure Geographic, depth, and age-related distribution Movements and migrations Stock structure and genetic studies Biology and ecology Reproduction Age and growth Diet Threats and status Silky sharks in tropical fisheries Stock assessment and fisheries management Conservation of silky sharks References

114 115 115 117 117 119 119 121 122 122 122 123 124 125

The Biology and Ecology of the Oceanic Whitetip Shark, Carcharhinus longimanus Ramón Bonfil, Shelley Clarke and Hideki Nakano

128

Introduction Distribution and movements

128 129

Contents

12

13

xi

Biology and ecology Diet Reproduction Age and growth Demographic analyses Fisheries Catch and catch-rate data Utilization Management and conservation Acknowledgments References

131 131 131 132 133 134 134 135 136 137 137

The Biology and Ecology of the Blue Shark, Prionace glauca Hideki Nakano and John D. Stevens

140

Introduction Biology and ecology Age and growth Reproduction Diet Distribution and movements Distribution Migration and movements Threats and status Fisheries Population status Acknowledgments References

140 141 141 141 142 143 143 143 145 145 147 148 148

The Biology and Ecology of the Pelagic Stingray, Pteroplatytrygon violacea (Bonaparte, 1832) Julie A. Neer

152

Introduction Biology and ecology Distribution and movements Threats and status Conclusions Acknowledgments References

152 153 155 157 157 158 158

Part III Trends in Catches and Abundance of Pelagic Sharks Introduction Description of fisheries and catch data

161 163 163

xii

Contents

Abundance trends from catch-rate data Recommendations References 14

15

16

164 165 165

A Global Overview of Commercial Fisheries for Open Ocean Sharks Merry D. Camhi, Elizabeth Lauck, Ellen K. Pikitch and Elizabeth A. Babcock

166

Introduction Data limitations and collection efforts Global elasmobranch catches Pelagic sharks in Atlantic Ocean fisheries Pelagic sharks in Pacific Ocean fisheries Pelagic sharks in Indian Ocean fisheries A catalog of pelagic-shark-fishing nations Major pelagic-shark-fishing nations Moderate pelagic-shark-fishing nations Discussion Acknowledgments References

166 167 170 172 174 175 176 179 182 185 186 186

Recreational Fishing for Pelagic Sharks Worldwide Elizabeth A. Babcock

193

Introduction Information sources Recreational fishing by country Australia New Zealand United States United Kingdom Ireland Canada South Africa Italy Other countries Conclusions Acknowledgments References

193 194 194 194 197 198 200 200 200 201 201 201 201 202 202

Case Study: Blue and Mako Shark Catch Rates in US Atlantic Recreational Fisheries As Potential Indices of Abundance Gregory Skomal, Elizabeth A. Babcock and Ellen K. Pikitch

205

Introduction Methods

205 206

Contents

17

Results Discussion Acknowledgments References

207 209 211 211

Catches of Pelagic Sharks by Subsurface Longline Fisheries in the South Atlantic Ocean during the Last Century: A Review of Available Data with Emphasis on Uruguay and Brazil Fabio H. V. Hazin, Matt K. Broadhurst, Alberto F. Amorim, Carlos A. Arfelli and Andres Domingo

213

Introduction Catches of pelagic sharks by distant-water longline fleets Japan China Taiwan Korea Spain Catches of pelagic sharks by longline fleets from coastal nations Uruguay Brazil Factors influencing small-scale temporal and spatial trends in catches of blue shark Management of pelagic sharks and directions for future research Conclusions Acknowledgments References 18

19

xiii

214 215 215 215 215 216 216 216 217 219 223 225 226 226 227

Case Study: Blue Shark Catch-Rate Patterns from the Portuguese Swordfish Longline Fishery in the Azores Alexandre Aires-da-Silva, Rogério Lopes Ferreira and João Gil Pereira

230

Introduction Fishing seasons Standardized catch rates Length–frequency samples Conclusions Acknowledgments References

230 231 232 233 233 234 234

Case Study: Trends in Blue Shark Abundance in the Western North Atlantic As Determined by a Fishery-Independent Survey Robert E. Hueter and Colin A. Simpfendorfer

236

Introduction Survey catch records

236 237

xiv

20

21

22

23

Contents

Trends in abundance Acknowledgments References

238 240 241

Case Study: Elasmobranch Bycatch in the Pelagic Longline Fishery off the Southeastern United States, 1992–1997 Lawrence R. Beerkircher, Enric Cortés and Mahmood S. Shivji

242

Introduction Methods and Results Acknowledgments References

242 242 246 246

Pelagic Shark Fisheries in the Indian Ocean Malcolm J. Smale

247

Introduction Shark catches Commonly caught species Lamnidae Alopiidae Carcharhinidae Management and conservation Acknowledgments References

247 248 252 252 253 253 254 255 255

Case Study: The Bycatch of Pelagic Sharks in Australia’s Tuna Longline Fisheries John D. Stevens and Sally E. Wayte

260

Introduction Species composition Catch rates and catch Length and sex composition Stock status Acknowledgments References

260 261 262 265 267 267 267

Case Study: Catch and Management of Pelagic Sharks in Hawaii and the US Western Pacific Region Paul J. Dalzell, R. Michael Laurs and Wayne R. Haight

268

Introduction Catches and catch rates Stock status Economics and management Conclusions Acknowledgments References

268 269 271 272 273 273 273

Contents

24

Case Study: Pelagic Shark Fisheries along the West Coast of Mexico Oscar Sosa-Nishizaki, J. Fernando Márquez-Farías and Carlos J. Villavicencio-Garayzar

275

Introduction Artisanal fishery Pelagic longline fishery Gill-net fisheries Shrimp trawl bycatch Fisheries interactions and stock assessment Regulations Conclusions References

275 276 277 277 278 278 279 280 281

Part IV

25

26

xv

Methods to Improve Understanding of Pelagic Sharks: Demographics, Assessment, and Stock Structure Introduction Demography Stock structure and movement Stock assessment Conclusion

283 285 285 286 286 287

Intrinsic Rates of Increase in Pelagic Elasmobranchs Susan E. Smith, David W. Au and Christina Show

288

Introduction Methods Estimating the intrinsic rate of increase rZ(MSY) or rebound potential Choosing and applying life-history parameters Precision Results Discussion Acknowledgments References

288 290 290 291 292 292 292 294 294

Shark Productivity and Reproductive Protection, and a Comparison with Teleosts David W. Au, Susan E. Smith and Christina Show

298

Introduction Methods Estimating productivity Parameters of rebound potential Reproductive protection against collapse and time for recovery Results The mortality corresponding to MSY

298 299 299 299 302 303 303

xvi

27

28

29

Contents

Productivities: sharks and teleosts Reproductive protection against collapse and recovery times from depletion Discussion Acknowledgments References

303 304 306 306 306

Comparative Life History and Demography of Pelagic Sharks Enric Cortés

309

Introduction Methods Analysis of differences in life-history traits among species Estimation of population parameters and elasticities The simulation and projection process Results Differences in life-history traits among pelagic shark species Simulation of population parameters and elasticities, and position of the inflection point of population growth curves Discussion Links between life-history traits and population statistics of pelagic sharks: conservation and management implications Interpretation of rates of increase and the position of the inflection point of population growth curves Acknowledgments References

309 310 310 311 313 314 314 314 316 316 318 320 320

Molecular Markers and Genetic Population Structure of Pelagic Sharks Edward J. Heist

323

Introduction Molecular markers Genetic stock structure of pelagic sharks Conclusions Acknowledgments References

323 325 328 329 330 330

Case Study: Rapid Species Identification of Pelagic Shark Tissues Using Genetic Approaches Mahmood S. Shivji, Melissa Pank, Lisa J. Natanson, Nancy E. Kohler and Michael J. Stanhope Introduction General methods Case studies Conclusions

334

334 335 335 337

Contents

30

31

xvii

Acknowledgments References

337 338

Stock Structure of the Blue Shark (Prionace glauca) in the North Atlantic Ocean Based on Tagging Data Nancy E. Kohler and Patricia A. Turner

339

Introduction Methods Results and discussion Distribution of sizes and sex ratios Transregional movements Summary Acknowledgments References

339 341 341 342 342 347 348 348

Why Are Bayesian Methods Useful for the Stock Assessment of Sharks? Murdoch K. McAllister, Ellen K. Pikitch and Elizabeth A. Babcock

351

Introduction What should be the main goal of stock assessment for sharks? How has advice been provided for shark fishery management? Demographic analysis Fitting surplus production models to times-series of observations on relative abundance Age-structured, length-structured, or stage-structured modeling Some problems encountered with conventional assessment methods Compiling basic biological and fishery data Integrating different types of data and results Reconciling contradictory data, information, and results Thoroughly accounting for uncertainty Conveying uncertainty in a meaningful way to decision makers How should uncertainty be dealt with in stock assessment? Identify alternative plausible hypotheses Evaluate the weight of evidence in support of each hypothesis Use decision tables without mathematical probabilities Bayesian methods Bayes’ theorem Example: National Marine Fisheries Service assessment of Atlantic coastal sharks A Bayesian stock assessment of Atlantic large coastal sharks Recommendations for learning Bayesian stock assessment methods Conclusions Acknowledgments References

351 352 352 352 354 355 355 355 356 356 356 357 357 358 358 358 359 359 361 361 363 364 364 364

xviii

32

Contents

Embracing Movement and Stock Structure for Assessment of Galeorhinus galeus Harvested off Southern Australia Terence I. Walker, Bruce L. Taylor, Lauren P. Brown and André E. Punt

369

Introduction Stock structure and movement patterns Spatially aggregated stock assessment Stock assessment incorporating movement rates and stock structure Movement simulation model Spatially structured stock assessment model Movement estimation within an integrated tag model Conclusions Appendix: movement estimation within an integrated tag model Model parameters Likelihood function Movement and survival Mortality Growth Acknowledgments References

369 373 374 375 376 377 377 384 385 385 386 386 387 388 388 389

Part V

33

34

Conservation and Management Outlook for Pelagic Sharks Introduction Data collection and assessment Shark fishery management New technologies Conclusion

393 395 395 395 396 396

Conservation Status of Pelagic Elasmobranchs Merry D. Camhi

397

Introduction Threats Conservation status Discussion Acknowledgments References

397 398 400 410 412 412

Domestic and International Management for Pelagic Sharks Merry D. Camhi, Sonja V. Fordham and Sarah L. Fowler

418

Introduction Management tools available for pelagic sharks Fishing restrictions

418 419 420

Contents

Prohibitions on finning Species protections International and regional management action Fisheries agreements Wildlife conservation agreements Domestic management action Conclusions Recommendations Acknowledgments References 35

36

The Rise and Fall (Again) of the Porbeagle Shark Population in the Northwest Atlantic Steven E. Campana, Warren Joyce, Linda Marks, Peter Hurley, Lisa J. Natanson, Nancy E. Kohler, Christopher F. Jensen, Joseph J. Mello, Harold L. Pratt Jr., Sigmund Myklevoll and Shelton Harley

xix

420 423 425 425 430 433 437 438 439 439

445

Introduction Fishery and population dynamics The fishery Trends in length and age composition Commercial catch rates Estimation of rates of natural and total mortality Recent mortality rates based on Paloheimo Z’s Petersen calculations of abundance and exploitation rate Yield per recruit Age- and sex-structured population model Discussion Acknowledgments References

445 446 446 449 450 450 453 453 454 455 455 459 460

Methods to Reduce Bycatch Mortality in Longline Fisheries Daniel L. Erickson and Steven A. Berkeley

462

Introduction Methods Gulf of Mexico pelagic longline experiment Gulf of Alaska demersal longline experiment Results Gulf of Mexico pelagic longline experiment Gulf of Alaska demersal longline experiment Discussion Acknowledgments References

462 463 463 464 465 465 467 468 470 470

xx

37

38

Index

Contents

Data Collection, Research, and Assessment Efforts for Pelagic Sharks by the International Commission for the Conservation of Atlantic Tunas Elizabeth A. Babcock and Hideki Nakano

472

Introduction Assessment of blue and shortfin mako sharks Conclusions References

472 474 476 477

Pelagic Sharks and the FAO International Plan of Action for the Conservation and Management of Sharks Rachel D. Cavanagh, Sarah L. Fowler and Merry D. Camhi

478

Introduction Progress Discussion Lack of political will Lack of technical capacity Lack of resources Pelagic sharks and the IPOA Summary Acknowledgments References

478 481 485 485 486 486 487 488 489 489 493

List of Contributors

Alexandre Aires-da-Silva Inter-American Tropical Tuna Commission 8604 La Jolla Shores Drive La Jolla, CA 92037, USA Tel: ⫹1 858 546 7022 Email: [email protected] Alberto F. Amorim Pólo Especializado de Desenvolvimento Tecnológico do Agronegócio do Pescado Marinho Instituto de Pesca Av. Bartolomeu de Gusmão 192 Santos, São Paulo, Brasil Tel: ⫹55 13 261 5995 Email: [email protected] Scot D. Anderson P.O. Box 390 Inverness, CA 94937, USA Tel: ⫹1 415 669 1077 Email: [email protected] Carlos A. Arfelli Pólo Especializado de Desenvolvimento Tecnológico do Agronegócio do Pescado Marinho Instituto de Pesca Av. Bartolomeu de Gusmão 192 Santos, São Paulo, Brasil Tel: ⫹55 13 261 5995 Email: [email protected] David W. Au Southwest Fisheries Science Center NOAA/National Marine Fisheries Service 10954 Red Rock Drive San Diego, CA 92131, USA Tel: ⫹1 858 566 2935 Email: [email protected]

Elizabeth A. Babcock Pew Institute for Ocean Science Rosenstiel School of Marine and Atmospheric Science University of Miami 4600 Rickenbacker Causeway Miami, FL 33149, USA Tel: ⫹1 305 421 4852 Email: [email protected] Lawrence R. Beerkircher NOAA/National Marine Fisheries Service Southeast Fisheries Science Center Miami Lab 75 Virginia Beach Drive Miami, FL 33149, USA Tel: ⫹1 305 361 4290 Email: [email protected] Steven A. Berkeley (deceased) University of California Santa Cruz Long Marine Laboratory 100 Shaffer Road Santa Cruz, CA 95060, USA Barbara A. Block Tuna Research and Conservation Center Stanford University Hopkins Marine Station Oceanview Boulevard Pacific Grove, CA 93950, USA Tel: ⫹1 831 655 6236 Email: [email protected] Ramón Bonfil 351 East Fourth Street, Apartment 1D New York, NY 10009, USA Tel: ⫹1 212 473 2808 Email: [email protected]

xxii

List of Contributors

Andre M. Boustany Nicholas School of the Environment and Earth Sciences Duke University P.O. Box 90328 Durham, NC 27708, USA Tel: ⫹1 919 613 8021 Email: [email protected] Matt K. Broadhurst NSW DPI, Fisheries Conservation Technology Unit P.O. Box J321 Coffs Harbour, NSW 2450, Australia Tel: ⫹61 2 6648 3905 Email: [email protected] Lauren P. Brown Primary Industries Research Victoria P.O. Box 114 Queenscliff, Victoria 3225, Australia and Department of Zoology University of Melbourne Parkville, Victoria 3052, Australia Tel: ⫹61 3 5258 0111 Email: [email protected] Barry D. Bruce CSIRO Marine and Atmospheric Research P.O. Box 1538 Hobart 7000, Tasmania, Australia Tel: ⫹1 61 6232 5413 Email: [email protected] George H. Burgess Florida Program for Shark Research Florida Museum of Natural History University of Florida Gainesville, FL 32611, USA Tel: ⫹1 352 392 1721 x471 Email: [email protected] Gregor M. Cailliet Moss Landing Marine Laboratories 8272 Moss Landing Road Moss Landing, CA 95039, USA Tel: ⫹1 831 771 4432 Email: [email protected]

Merry D. Camhi 126 Raymond Street Islip, NY 11751, USA Tel: ⫹1 631 581 9011 Email: [email protected] Steven E. Campana Population Ecology Division Bedford Institute of Oceanography P.O. Box 1006 Dartmouth, Nova Scotia, Canada B2Y 4A2 Tel: ⫹1 902 426 3233 Email: [email protected] Rachel D. Cavanagh British Antarctic Survey High Cross Madingley Road Cambridge CB3 0ET, UK Tel: ⫹44 (0) 1223 221 470 Email: [email protected] Shelley Clarke National Research Institute of Far Seas Fisheries Fisheries Agency of Japan 5-7-1 Shimizu-Orido Shizuoka, 424 8633 Japan Tel: ⫹81 543 36 6046 Email: [email protected] Leonard J. V. Compagno Shark Research Center Iziko – South African Museum P.O. Box 61, 25 Queen Victoria Street Cape Town, South Africa 8000 Tel: ⫹27 21 481 3859 Email: [email protected], [email protected] Enric Cortés Southeast Fisheries Science Center NOAA/National Marine Fisheries Service Panama City Laboratory 3500 Delwood Beach Road Panama City, FL 32408, USA Tel: ⫹1 850 234 6541 x220 Email: [email protected]

List of Contributors

Paul J. Dalzell Western Pacific Regional Fishery Management Council 1164 Bishop Street, Suite 1400 Honolulu, HI 96813, USA Tel: ⫹1 808 522 6042 Email: [email protected] Andres Domingo Area de Recursos Pelágicos Instituto Nacional de Pesca Constituyente 1497 Montevideo 11200, Uruguay Tel: ⫹598 2404689 Email: [email protected], [email protected] Daniel L. Erickson Pew Institute for Ocean Science 541 Willamette Street, Suite 207A Eugene, OR 97401, USA Tel: ⫹1 541 302 3234 Email: [email protected] Rogério Lopes Ferreira Departamento de Oceanografia e Pescas Universidade dos Açores PT 9901 862, Horta, Portugal Sonja V. Fordham The Shark Alliance and The Ocean Conservancy c/o Oceana, Rue Montoyer, 39 1000 Brussels, Belgium Tel: ⫹32 25 132242 Email: [email protected] Sarah L. Fowler Naturebureau International 36 Kingfisher Court Hambridge Road Newbury Berkshire RG14 5SJ, UK Tel: ⫹44 (0) 1635 550380 Email: [email protected]

xxiii

Malcolm P. Francis National Institute of Water and Atmospheric Research Private Bag 14901 Wellington, New Zealand Tel: ⫹64 4 386 0300 Email: [email protected] Kenneth J. Goldman Alaska Department of Fish and Game 3298 Douglas Place Homer, AK 99603, USA Tel: ⫹1 907 235 8191 Email: [email protected] Wayne R. Haight Hawaii Division of Aquatic Resources Papahanaumokuakea Marine National Monument 6600 Kalaniana’ole Highway, Suite 300 Honolulu, HI 96825, USA Tel: ⫹1 808 397 2660 x247 Email: [email protected] Shelton Harley Ministry of Fisheries P.O. Box 1020 Wellington, New Zealand Tel: ⫹64 4 819 4267 Email: [email protected] Fabio H. V. Hazin Universidade Federal Rural de Pernambuco – UFRPE Departamento de Pesca Laboratório de Oceanografia Pesqueira Av. Dom Manuel de Medeiros s/n Dois Irmãos Recife-PE Brazil, CEP 52.171-900 Tel: ⫹55 81 441 7276 Email: [email protected] Edward J. Heist Fisheries and Illinois Aquaculture Center Southern Illinois University 173 Life Science II, 1125 Lincoln Drive Carbondale, IL 62901, USA Tel: ⫹1 618 536 7761 Email: [email protected]

xxiv

List of Contributors

Robert E. Hueter Center for Shark Research Mote Marine Laboratory 1600 Ken Thompson Parkway Sarasota, FL 34236, USA Tel: ⫹1 941 388 4441 x323 Email: [email protected]

R. Michael Laurs RML Fisheries Oceanographer Consultant, LLC 555 Grove Street Jacksonville, OR 97530, USA Tel: ⫹1 541 899 9091 Email: [email protected]

Peter Hurley Population Ecology Division Bedford Institute of Oceanography P.O. Box 1006 Dartmouth, Nova Scotia, Canada B2Y 4A2 Tel: ⫹1 902 426 3520 Email: [email protected]

Linda Marks Population Ecology Division Bedford Institute of Oceanography P.O. Box 1006 Dartmouth, Nova Scotia, Canada B2Y 4A2 Tel: ⫹1 902 426 4435 Email: [email protected]

Christopher F. Jensen Northeast Fishery Science Center NOAA/National Marine Fisheries Service 28 Tarzwell Drive Narragansett, RI 02882, USA Warren Joyce Population Ecology Division Bedford Institute of Oceanography P.O. Box 1006 Dartmouth, Nova Scotia, Canada B2Y 4A2 Tel: ⫹1 902 426 6382 Email: [email protected] Nancy E. Kohler Northeast Fishery Science Center NOAA/National Marine Fisheries Service 28 Tarzwell Drive Narragansett, RI 02882, USA Tel: ⫹1 401 782 3332 Email: [email protected] Elizabeth Lauck Conservation International 2300 Southern Boulevard Bronx, NY 10460, USA Tel: ⫹1 718 220 2151 Email: [email protected]

J. Fernando Márquez-Farías Instituto Nacional de la Pesca, Programa Tiburón Calle 20 Sur #605 Guaymas, Sonora, México, C.P. 85400 Email: [email protected] Murdoch K. McAllister Fisheries Center Aquatic Ecosystems Research Laboratory 2202 Main Mall University of British Columbia Vancouver, BC, Canada V6T 1Z4 Tel: ⫹1 604 822 8934 Email: [email protected] Joseph J. Mello Northeast Fishery Science Center NOAA/National Marine Fisheries Service 28 Tarzwell Drive Narragansett, RI 02882, USA Tel: ⫹1 508 495 2110 Email: [email protected] John A. Musick College of William & Mary School of Marine Science Virginia Institute of Marine Science P.O. Box 1346 Gloucester Point, VA 23062, USA Tel: ⫹1 804 684 7317 Email: [email protected]

List of Contributors

Sigmund Myklevoll Institute of Marine Research P.O. Box 1870 Nordnes, 5817 Bergen, Norway Tel: ⫹47 55 23 86 96 Email: [email protected]

João Gil Pereira Departamento de Oceanografia e Pescas Universidade dos Açores PT 9901 862, Horta, Portugal Tel: ⫹351 292 200 431 Email: [email protected]

Hideki Nakano National Research Institute of Far Seas Fisheries Fisheries Agency of Japan 5-7-1 Shimizu-Orido Shizuoka, 424 8633 Japan Tel: ⫹81 543 36 6046 Email: [email protected]

Ellen K. Pikitch Pew Institute for Ocean Science Rosenstiel School of Marine and Atmospheric Science 125 East 56th Street New York, NY 10022, USA Tel: ⫹1 212 756 0042 Email: [email protected]

Lisa J. Natanson Northeast Fisheries Science Center NOAA/National Marine Fisheries Service 28 Tarzwell Drive Narragansett, RI 02882, USA Tel: ⫹1 401 782 3320 Email: [email protected]

Harold L. Pratt, Jr. Northeast Fisheries Science Center NOAA/National Marine Fisheries Service 28 Tarzwell Drive Narragansett, RI 02882, USA

Julie A. Neer South Atlantic Fishery Management Council 4055 Faber Place #201 North Charleston, SC 29405, USA Tel: ⫹1 843 571 4366 Email: [email protected]

André E. Punt School of Aquatic and Fishery Sciences University of Washington P.O. Box 355020 Seattle, WA 98195, USA Tel: ⫹1 206 221 6319 Email: [email protected]

Melissa Pank Guy Harvey Research Institute Nova Southeastern University Oceanographic Center 8000 North Ocean Drive Dania Beach, FL 33004, USA

Peter Pyle Institute for Bird Populations P.O. Box 1346 Point Reyes Station, CA 94956, USA Tel: ⫹1 415 663 2053 Email: [email protected]

Daniel Pauly Fisheries Center Aquatic Ecosystems Research Laboratory 2202 Main Mall University of British Columbia Vancouver, BC, Canada V6T 1Z4 Tel: ⫹1 604 822 2731 Email: [email protected]

Darlene A. Ramon Southwest Fisheries Science Center NOAA/National Marine Fisheries Service 8604 La Jolla Shores Drive La Jolla, CA 92037, USA Tel: ⫹1 858 546 7074 Email: [email protected]

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List of Contributors

Randall C. Rasmussen Southwest Fisheries Science Center NOAA/National Marine Fisheries Service 8604 La Jolla Shores Drive La Jolla, CA 92037, USA Tel: ⫹1 858 546 7184 Email: [email protected] Brenda L. Roman Florida Program for Shark Research Florida Museum of Natural History University of Florida Gainesville, FL 32611, USA Mahmood S. Shivji Guy Harvey Research Institute Nova Southeastern University Oceanographic Center 8000 North Ocean Drive Dania Beach, FL 33004, USA Tel: ⫹1 954 262 3653 Email: [email protected] Christina Show Southwest Fisheries Science Center NOAA/National Marine Fisheries Service 8604 La Jolla Shores Drive La Jolla, CA 92037, USA Tel: ⫹1 858 546 7078 Email: [email protected] Colin A. Simpfendorfer Fishing and Fisheries Team School of Earth and Environmental Sciences James Cook University Townsville, Queensland 4811, Australia Tel: ⫹61 (07) 4781 5287 Email: [email protected] Gregory Skomal Massachusetts Division of Marine Fisheries Massachusetts Shark Research Program Martha’s Vineyard Research Station P.O. Box 68 Vineyard Haven, MA 02568, USA Tel: ⫹1 508 693 4372 Email: [email protected]

Malcolm J. Smale Bayworld Centre for Research and Education Port Elizabeth Museum at Bayworld P.O. Box 13147 Humewood, South Africa 6013 Tel: ⫹27 041 584 0650 Email: [email protected] Susan E. Smith Seiurus Biological Consulting 13716 Ruette le Parc, Suite #E Del Mar, CA 92014, USA Tel: ⫹1 858 350 8936 Email: [email protected] Franklin F. Snelson, Jr. Florida Program for Shark Research Florida Museum of Natural History University of Florida Gainesville, FL 32611, USA Tel: ⫹1 352 392 1721 Email: [email protected] Oscar Sosa-Nishizaki Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE) Apartado postal 2732 Ensenada, Baja California México, C.P. 22800 Tel: ⫹52 646 1750540 Email: [email protected] Michael J. Stanhope Department of Population Medicine and Diagnostic Sciences College of Veterinary Medicine Cornell University Ithaca, NY 14853, USA Tel: ⫹1 607 253 4136 Email: [email protected] John D. Stevens CSIRO Marine and Atmospheric Research P.O. Box 1538 Hobart 7000, Tasmania, Australia Tel: ⫹ 61 3 6232 5353 Email: [email protected]

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Bruce L. Taylor Primary Industries Research Victoria P.O. Box 114 Queenscliff, Victoria 3225, Australia and Department of Zoology University of Melbourne Parkville, Victoria 3052, Australia Tel: ⫹61 3 5258 0111 Email: [email protected]

Terence I. Walker Primary Industries Research Victoria P.O. Box 114 Queenscliff, Victoria 3225, Australia and Department of Zoology University of Melbourne Parkville, Victoria 3052, Australia Tel: ⫹61 3 5258 0111 Email: [email protected]

Patricia A. Turner Northeast Fisheries Science Center NOAA/National Marine Fisheries Service 28 Tarzwell Drive Narragansett, RI 02882, USA Tel: ⫹1 401 782 3330 Email: [email protected]

Sally E. Wayte CSIRO Marine and Atmospheric Research P.O. Box 1538 Hobart 7000, Tasmania, Australia Tel: ⫹61 03 6232 5464 Email: [email protected]

Carlos J. Villavicencio-Garayzar Departamento de Biología, UABCS Carretera al Sur Km 5.5 La Paz, Baja California Sur Mexico, C.P. 23080 Email: [email protected]

Kevin C. M. Weng School of Ocean and Earth Science and Technology University of Hawaii at Manoa 1000 Pope Road Honolulu, HI 96822, USA Tel: ⫹1 808 956 6346 Email: [email protected]

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Series Foreword

“You may rest assured that the British Government is entirely opposed to sharks” (Winston Churchill, 1945, in response to a parliamentary question about developing shark repellents) Sharks are just too toothy for their own good. The popular image conjured up by Jaws films, and Hawaiian kings who used human bait for shark fishing, has exacerbated the image problem that must be addressed by those attempting the conservation of sharks. Indeed, there has been some success here: Their public image has definitely changed since American shark researchers termed brightly-coloured life preserver jackets “yum-yum yellow.” But the sharks have not changed of course; they seem to have been pretty much the same since the Jurassic. What’s not the same though, is that in the last 25 years, the mere blink of an eye in shark history, many species have been so overexploited that local extinctions have been documented, and worldwide, most large long-lived sharks appear to be at least 90% depleted. We are only just beginning to guess at the ecosystem consequences of these changes. In classical times, sharks were both admired and feared. In the 2nd century AD, the Graeco-Roman poet Oppian praised the parental instincts of the live-bearing blue shark (Mair, 1928). Five hundred years earlier, Herodotus recounts how the ancient Greeks liked the way that sharks ate a lot of shipwrecked Persians: “… starting from Acanthos [the Persian fleet] attempted to get round Mount Athos; but as they sailed round, there fell upon them a violent North Wind, against which they could do nothing, and handled them very roughly, casting away very many of their ships on Mount Athos. It is said indeed that the number of the ships destroyed was three hundred, and more than twenty thousand men; for as this sea which is about Athos is very full of sharks, some were seized and devoured by these and so perished, while others were dashed against the rocks.” (Herodotus, History, Book 6: 44; Macaulay, 1914) Herodotus’ story is echoed in modern times. After the U.S.S. Indianapolis was torpedoed near Tinian Island in the Western Pacific on 30 July 1945, sharks ate more than 900 men in the three days before rescuers arrived: Only 318 crew were saved. In an ironic twist worthy of a Greek tragedy, rescue was delayed because few knew that the cruiser was there: It had just completed a top secret mission delivering the heavy bits of three atomic bombs, two of which were dropped on Hiroshima and Nagasaki exactly one week later. This book, whose 38 chapters derive originally from a workshop held in 2000 that attracted over a hundred of the world’s top shark specialists, aims in five sections to consolidate and expand our knowledge of open ocean, pelagic sharks. The three chapters of

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Series Foreword

Part I cover the diversity and reproductive biology of pelagic sharks. Part II contains ten chapters that set out systematic accounts of the biology and ecology of nine of the principal pelagic shark species, presenting much synoptic information that is new. Part III has nineteen chapters that set out what is known (and not known) about the fishery catches of sharks worldwide. Bycatch in longline fisheries is especially serious and many sharks that are caught are unidentified and unreported. Indeed, sharks constitute only 2% of reported fishery catches on the high seas (areas outside the Exclusive Economic Zones of countries), but the true figure must be many times larger, as evidenced by calculations made from fins sold in Asian markets. The eight chapters in Part IV document the life histories of pelagic sharks, compare them with bony fish and describe genetic tags and markers that can help reveal stock structures. The book closes with Part V, which includes five chapters that review ongoing, but as yet only partially successful, efforts to conserve sharks. Fortunately, shark conservation does seem to be becoming more popular. For example, under pressure from environmental organisations, in 2005 Disney World in Hong Kong stopped selling shark fin soup, a tasteless, glutinous but expensive dish popular in wedding celebrations but held by many to be responsible for much of the shark decline worldwide. Such welcome actions seem to be spreading in Asia; in September 2007, the Natural Resources and Environment Minister from Malaysia, Azmi Khalid, banned shark fin soup from official function menus. Back in the Second World War, a young lady called Julia Child was recruited to Allied intelligence; she seemed to have talents with food, so her first job was to develop a recipe for shark repellent. It didn’t work too well: What repelled sharks in the aquarium tank piqued their curiosity and actually attracted sharks in the sea. But Ms. Child went on to become a famous food guru and the successful author of many cookery books. As Series Editor I trust that this timely and informative book on sharks of the open ocean will be just as popular as those cookery books, will attract readers, and will encourage conservation of these ancient, magnificent (and still slightly scary, toothy) creatures. Professor Tony J. Pitcher Editor, Blackwell Publishing Fish and Aquatic Resources Series Fisheries Centre, University of British Columbia, Vancouver, Canada October 2007 References cited Mair, A.W. (1928) Oppian, Colluthus, Tryphiodorus. Loeb Classical Library, Heinemann, UK. 635pp. Macaulay, G.C. (1914) The History of Herodotus, Translated (3rd edition). MacMillan and Co. Limited, St. Martin’s Street, London, UK. Book 6: 44 (Project Gutenberg).

Series Rationale Fish researchers (a.k.a. fish freaks) like to explain, to the bemused bystander, how fish have evolved an astonishing array of adaptations; so much so that it can be difficult for them to comprehend why anyone would study anything else. Yet, at the same time, fish are among the last wild creatures on our planet that are hunted by humans for sport or food. As a consequence, today we recognize that the reconciliation of exploitation with the conservation of biodiversity provides a major challenge to our current scientific knowledge

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and expertise. Even evaluating the trade-offs that are needed is a difficult task. Moreover, solving this pivotal issue calls for a multidisciplinary consilience of fish physiology, biology and ecology with social sciences such as economics and anthropology in order to probe the frontiers of applied science. In addition to food, recreation (and inspiration for us fish freaks), it has, moreover, recently been realized that fish are essential components of aquatic ecosystems that provide vital services to human communities. Sadly, virtually all sectors of the stunning biodiversity of fishes are at risk from human activities. In freshwater, for example, the largest mass extinction event since the end of the dinosaurs has occurred as the introduced Nile perch in Lake Victoria eliminated over 100 species of endemic haplochromine fish. But, at the same time, precious food and income from the Nile perch fishery was created in a miserably poor region. In the oceans, we have barely begun to understand the profound changes that have accompanied a vast expansion of human fishing over the past 100 years. The Blackwell Series on Fish and Aquatic Resources is an initiative aimed at providing key, peer-reviewed texts in this fast-moving field.

Foreword

We have come a long way since our perception of sharks was shaped by films featuring World War II pilots downed in the Pacific and circled by ominous fins. Now, the images that come to mind are finless, bleeding shark carcasses being thrown overboard from fishing vessels or, more abstractly, plunging graphs documenting the decline of shark abundance throughout the world’s oceans. This important book will further change our perspective from sharks as menace to humans to sharks as yet another group of species that are being severely depleted by our ever-expanding fishing activities. Indeed, several pelagic sharks are threatened with endangerment and have already been added to the World Conservation Union’s (IUCN) Red List of Threatened Species. And one species, the white shark of man-eating lore, has recently been listed on CITES, the international treaty that monitors and controls trade in endangered species. Other sharks will follow if we do not quickly change our ways, notably by developing gears and fishing methods that, when targeting tuna and other fish, will spare sharks that are often the unintended bycatch. Approaches will also have to be found to deal with the shark fin soup issue: There are simply not enough fins on presently living and future sharks to feed the growing demand for a dish whose bland taste belies its bitter nature. In the meantime, we must improve our understanding of these fascinating animals – their movements, life histories, and distributions, their growth and mortality, and their behavior, perhaps one of the keys to designing more selective fishing gear. I had the pleasure of serving as keynote speaker at the International Pelagic Shark Workshop, held at the beautiful Asilomar oceanfront retreat in Pacific Grove, California, in February 2000, which eventually led to this book. Using then current knowledge, as incorporated in FishBase, the online encyclopedia of fishes, I presented a review of shark growth and natural mortality patterns that, I suggested, were regular enough to allow inferences on the life-history parameters of well-studied species to be applied to understudied species, via their maximum size and taxonomic affinities. By implication, this suggested that we should concentrate our research on other aspects of shark fisheries biology, such as mapping their catches, including the bycatch of various tuna fisheries and the catch of illegal fisheries. This book, introduced through the reviews of shark biodiversity, biology, and reproduction in Part I, shows that I was both a bit wrong, and a little bit right. I was wrong, in part, because the contributions in Part II – devoted to the growth, mortality, reproduction, and other aspects of the biology of 11 species of open ocean sharks – offer a wealth of new information, which will considerably improve our ability to make inferences about

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lesser-known species. The first three chapters in Part IV further enhance our understanding of pelagic sharks by providing specific and comparative life-history parameters for these species. Taken together, these contributions confirm that pelagic elasmobranchs, despite their wide distribution and the spectacular transoceanic migrations that some have exhibited, are extremely vulnerable to fishing, and that there is a critical need for protection of pelagic sharks and rays. I was a little bit right because, as Part III demonstrates, our knowledge of shark catches is scandalously limited. Although species-specific catch and discard data for pelagic sharks are still incomplete, the catch and bycatch studies herein begin to fill the information gap, especially as they cover not only the much-studied Atlantic, but also the Pacific and the often neglected Indian Ocean. The contributions in Part IV focus on methods to improve our understanding of pelagic sharks. They present a diverse set of tools, including demographic parameter analysis, genetic techniques, tagging methods and data analysis, and mathematical models for assessing stock structure, movements, and status. These contributions were included in the book because they are particularly useful for addressing the unique data constraints and life-history modes exhibited by pelagic sharks. The contributions in Part V confront the conservation and management outlook for pelagic sharks, and will be extremely useful to scientists, managers, and conservationists in government agencies, fishery groups, and nongovernmental organizations who are working to stop the widespread decline of pelagic shark populations. Yet I suspect one ingredient needs to be added to this mix: more public information and involvement. Pelagic sharks are wildlife, and they “belong” to everybody if they “belong” to anybody. Ultimately, it will be public revulsion at the sight of finned carcasses, of dead sharks entangled in drift nets, and of other needless killing that will determine the fate of sharks, just as strong public sentiment eventually forced governments to protect the great whales. An informed public is needed to stoke the political will to implement effective pelagic shark management. This book puts sound science in the hands of those who are responsible for ensuring that fishing is sustainable and that our oceans continue to support the life that they have spawned and nurtured for millions of years, including the lives of these beautiful animals. Daniel Pauly University of British Columbia, Vancouver, BC, Canada

Acknowledgments

The editors thank the people and organizations who helped organize the International Pelagic Shark Workshop in Pacific Grove, California, where the idea for this book was conceived. The Workshop was hosted by the Ocean Wildlife Campaign and its member organizations: National Audubon Society, National Coalition for Marine Conservation, Natural Resources Defense Council, Ocean Conservancy, Wildlife Conservation Society, and World Wildlife Fund. We thank David Wilmot, Russell Dunn, Liz Lauck, Sonja Fordham, Ken Hinman, Carl Safina, Lisa Speer, and Mike Sutton for many lively discussions and for their committed efforts to the conservation of the world’s sharks. Thanks go to Daniel Pauly for his insightful keynote address and for writing the book’s Foreword. We acknowledge the many advisors, speakers, and participants at the Workshop who contributed to this dynamic and spirited gathering, and we thank Kerri Kirvin and Bill Krol for their assistance in managing conference details. The Monterey Bay Aquarium provided a dramatic setting for the conference dinner. The Ocean Wildlife Campaign was supported by the Pew Charitable Trusts and The David and Lucile Packard Foundation. Many people have made contributions to this volume over its long gestation period even if they do not appear in name. We are most grateful to all the authors of the chapters for their valuable contributions and patience. We acknowledge those who have reviewed and commented on draft chapters: Their expert critiques demonstrably improved the quality of this book. Claudine Gibson and Susie Watts gave tremendous assistance in locating difficultto-find sources, and Shelley Clarke provided data and critical advice for a number of the chapters. Thanks go to our families and friends and, in particular, to Sonja Fordham and Shana Miller, who lent moral and general counsel along the way. Merry acknowledges the enduring support of Bev, Dana, Caren, Claudia, Debbie, and Pauline. Ellen and Beth thank Chris Santora and Ciani Mendez. We thank Nigel Balmforth, Kate Nuttall, and Laura Price at Wiley-Blackwell for their steady editorial assistance and patient understanding even as deadlines slipped. Finally, and most especially, we thank John Thomas, whose discerning eye and editorial perseverance made him much more than this volume’s exacting manuscript editor – he helped herd this sometimes reluctant beast toward the pasture gate of publication. Completion of this book would not have been possible without the financial support of the Pew Charitable Trusts through the Pew Institute for Ocean Science.

Part I

Introduction and Overview

Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

Chapter 1

Introduction to Sharks of the Open Ocean Ellen K. Pikitch, Merry D. Camhi and Elizabeth A. Babcock

Introduction The chondrichthyans, or cartilaginous fishes, are among the oldest extant taxa of vertebrates, having survived for more than 400 million years. Fishes that were morphologically similar to modern sharks swam in the seas when dinosaurs walked on land (Grogan and Lund, 2004). Cartilaginous fishes range from planktivores to apex predators, and exhibit every reproductive mode known in vertebrates, from egg laying to placental viviparity (Snelson et al., 2008). They are found throughout the world’s oceans – from coastal waters to the open ocean, from the surface to depths of 3,000 m (Priede et al., 2006). Of the roughly 1,160 extant species of cartilaginous fishes, 26–31 species (about 2.5%) are oceanic (Compagno, 2008), spending much of their life in open ocean waters away from continental landmasses. Oceanic waters are generally less productive and contain less biomass and less diversity than coastal waters. Nevertheless, there are also hot spots of relatively high productivity and biodiversity in the open ocean, generally associated with nearby structures such as seamounts, as well as areas where eddies frequently form (Worm et al., 2003). Areas of high productivity can vary seasonally, or shift with oceanographic conditions, so that it is necessary for tuna, billfishes, sharks, turtles, seabirds, and other large animals of the high seas to migrate long distances (Block et al., 2001). The open ocean sharks are particularly well adapted to this changing environment, possessing the ability to migrate across ocean basins. For example, blue sharks (Prionace glauca, Carcharhinidae) routinely cross the Atlantic (Kohler and Turner, 2008), and white sharks (Carcharodon carcharias, Lamnidae) tagged off the Pacific Coast of North America have traveled to the Hawaiian Islands (Boustany et al., 2002, 2008) and from South Africa to Western Australia (Bonfil, 2005). The oceanic species also tend to produce larger litter sizes than related coastal species, which Snelson et al. (2008) suggest may be an adaptation to the scarce and patchy food resources in the open ocean. These large litter sizes do not make them more productive than other sharks; rather, the oceanic species fall into the middle of the range of shark productivities (Smith et al., 2008a). While there are far fewer species of elasmobranchs (sharks and rays) in the open ocean than in coastal waters, these species are wide-ranging and relatively numerous, and play an important role in the food webs of the high seas. Sharks are the apex predators of the open Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

4

Sharks of the Open Ocean

ocean, feeding on tunas, other fishes, and squid. Historically, they were quite common in the high seas and were caught in most fishing operations. In high-seas fisheries for tunas and swordfish, the most common bycatch species are sharks – often blue and silky (Carcharhinus falciformis, Carcharhinidae) sharks (Williams, 1999; Beerkircher et al., 2008; Hazin et al., 2008). Many recent studies have demonstrated declines in the biomass of top predators, including sharks, throughout the world’s oceans (Friedlander and DeMartini, 2002; Myers and Worm, 2003; Hutchings and Reynolds, 2004). Given the potential importance of apex predators in structuring marine food webs (Estes et al., 1998), there is a critical need for increased understanding of the biology, current status, and ecological role of oceanic sharks. These species have received less research attention than their coastal relatives, in part because of the difficulty of studying wide-ranging animals that spend most of their lives far from land.

The need for oceanic shark research and management In 2000, the editors of this book and the Ocean Wildlife Campaign convened a symposium on open ocean sharks, called the International Pelagic Shark Workshop, in Pacific Grove, California. At that time, large and expanding high-seas fisheries (Fig. 1.1) were killing hundreds of thousands of sharks a year as both directed catch and bycatch, yet few studies had been conducted on the biology of oceanic sharks or their capacity to sustain these fisheries. Although the ranges of oceanic sharks often overlap the 200-nautical-mile exclusive economic zones of coastal nations, where there is some potential for management, many of these sharks are also caught in international waters, where shark fishing is generally not regulated. Open ocean sharks are apex predators and, like virtually all chondrichthyans, have a limited ability to sustain fisheries.

16

Other fishes and invertebrates

Catches (x1,000,000 t)

14

Sharks and rays

12

Tuna and billfishes

10 18 6 4 2

2000

1995

1990

1985

1980

1975

1970

1965

1960

1955

1950

0

Year Fig. 1.1 Total fish catches in the high seas, defined as all areas not included in the exclusive economic zones (i.e., within 200 nautical miles of the coast) of any country, from 1950 to 2001 (Watson et al., 2004; Pauly, 2005).

Introduction to Sharks of the Open Ocean

5

One of the few well-studied populations of oceanic sharks was that of the Northwest Atlantic porbeagle (Lamna nasus, Lamnidae). This population had collapsed in the 1960s from severe overfishing, and had recovered somewhat during the 1980s. Since the 1990s, the porbeagle population has declined to the lowest levels on record, despite the fishery being strictly controlled under a management plan that is intended to be precautionary (Campana et al., 2008). We were concerned that other pelagic sharks with similar life histories might also be experiencing unsustainable fishing pressure, and decided a symposium would help highlight the research and management needs for these species. The International Pelagic Shark Workshop brought together 130 fishery scientists, managers, and conservationists from 12 countries. The Workshop objectives were to collate all available biological and fishery data for oceanic sharks subject to fisheries and to identify additional data and analyses required for assessment and for the purposes of fishery management. We focused on 12 oceanic pelagic and coastal/outer-shelf pelagic species of special management concern from four families: Alopiidae – pelagic thresher (Alopias pelagicus), bigeye thresher (A. superciliosus), and common thresher (A. vulpinus); Lamnidae – shortfin mako (Isurus oxyrinchus), longfin mako (I. paucus), salmon shark (Lamna ditropis), and porbeagle (L. nasus); Carcharhinidae – silky (Carcharhinus falciformis), oceanic whitetip (C. longimanus), and blue shark (P. glauca); and Dasyatidae – pelagic stingray (Pteroplatytrygon violacea) (Table 1.1). The white shark (Carcharodon carcharias, Lamnidae) was added later when evidence of its oceanic migrations was published (Boustany et al., 2002, 2008). The Workshop raised awareness of the conservation status and management gaps for these high-seas oceanic species. It also served to focus and accelerate research and conservation measures by scientists, fishing nations, and regional fisheries management organizations, whose subsequent findings and actions are reflected in the chapters in this volume. Sharks of the Open Ocean is organized into five parts: (1) Introduction and Overview; (2) Life History and Status of Pelagic Elasmobranchs; (3) Trends in Catches and Abundance of Pelagic Sharks; (4) Methods to Improve Understanding of Pelagic Sharks: Demographics, Assessment, and Stock Structure; and (5) Conservation and Management Outlook for Pelagic Sharks. Each part begins with an introduction written by the editors. Some

Table 1.1 Elasmobranch species addressed in Sharks of the Open Ocean. Common name

Scientific name

Pelagic thresher Bigeye thresher Common thresher White shark Shortfin mako Longfin mako Salmon shark Porbeagle Silky shark Oceanic whitetip shark Blue shark Pelagic stingray

Alopias pelagicus Alopias superciliosus Alopias vulpinus Carcharodon carcharias Isurus oxyrinchus Isurus paucus Lamna ditropis Lamna nasus Carcharhinus falciformis Carcharhinus longimanus Prionace glauca Pteroplatytrygon violacea

6

Sharks of the Open Ocean

commercially important coastal species (e.g., dusky, Carcharhinus obscurus; hammerheads, Sphyrna spp.; and tiger sharks, Galeocerdo cuvier) move offshore and are taken regularly in pelagic fisheries. These species, however, as well as other noncommercial pelagic and semipelagic elasmobranchs (Compagno, 2008), are not addressed in this volume, except in a comparative demographic study (Smith et al., 2008a) and in a chapter describing an assessment of school sharks (Galeorhinus galeus, Triakidae; Walker et al., 2008), which was included as a demonstration of a spatially explicit stock assessment method that would be useful for oceanic sharks. It should also be noted that we have not been strict in the use of the terms “oceanic” and “pelagic” in reference to open ocean sharks, allowing authors to use these terms interchangeably (although see Compagno, 2008, for definitions of the terms).

Evaluating the conservation status of open ocean sharks Compared to the coastal sharks, and to the tunas caught in high-seas fisheries, the oceanic sharks have not been well studied: Data on catches, abundance trends, and life history are quite limited. These data are necessary to determine whether current fishing levels are sustainable and to develop a strategy to conserve and manage oceanic shark populations. Most importantly, we need to know how many sharks of each species are being killed in fisheries, at least in recent years, but preferably over the entire history of the fishery. In general, once catches are known, there are several ways to determine whether they are sustainable. An index of abundance, such as a survey or the catch rates in a fishery (which can be proportional to abundance), can be used to assess whether the historical catches caused a given population to decline, and if so, by how much. A population dynamics model fitted to the abundance and catch data can be used to ascertain what level of catch is sustainable, and whether catches need to be reduced to allow the population to rebuild to a healthy level. This is the method most commonly used in fisheries stock assessment and management (Campana et al., 2008; McAllister et al., 2008; Walker et al., 2008). It is also common to use demographic methods, which use age-specific estimates of fecundity, natural mortality, and fishing mortality (Au et al., 2008; Cortés, 2008; Smith et al., 2008a), to evaluate a population’s vulnerability to fishing pressure. Such methods can determine the relative vulnerability of different species, and can determine which life stages need the greatest protection. Methods that combine abundance indices and demographic data can also be used to evaluate the sustainability of fisheries (McAllister et al., 2008). Our ability to apply these fishery assessment methods to oceanic sharks, however, is stymied by data limitations, particularly on total landings and discards. Although sharks are commonly caught in high-seas fisheries, they are often caught incidentally in fisheries targeting tunas or swordfish. Because of this, shark catches have generally not been reported, or have been reported as “unidentified sharks” instead of by species (Camhi et al., 2008a; Smale, 2008). A recent study of the shark fin trade found that the current catches of some species, such as blue and shortfin mako, are much higher than the landings reported to the Food and Agriculture Organization (FAO) and the regional fishery management organizations (Clarke, 2003; Clarke et al., 2006). Of the shark fins traded in Hong Kong, 17% (by weight) were from blue sharks; fins from silky, shortfin mako, threshers, and oceanic whitetip were

Introduction to Sharks of the Open Ocean

7

also common. The estimated numbers of pelagic sharks killed annually to support this trade were 4.6–15.8 million blue sharks, 400,000–2,000,000 silky, 200,000–1,200,000 oceanic whitetip, 300,000–1,000,000 shortfin mako, and 400,000–3,900,000 threshers (Clarke et al., 2006). The shark catches reported to regional fishery management organizations have been increasing over the last decade, although it is not clear how much of the increase represents an actual increase in catches and how much is simply due to better reporting (Babcock and Nakano, 2008; Smale, 2008). In any case, these large catches may or may not be sustainable for species with life histories more similar to those of marine mammals than to the bony fishes that are caught in high-seas fisheries (Camhi et al., 1998). Despite the lack of reliable catch data, several recent studies have evaluated changes in oceanic shark abundance over time to determine whether fisheries have caused their depletion. Survey data have shown declines in male blue sharks in the Northwest Atlantic (Hueter and Simpfendorfer, 2008). Studies of shark catch rates from commercial fisheries have found declines of thresher, blue, mako, and oceanic whitetip sharks in the Northwest Atlantic (Baum et al., 2003), although Nakano (1996) found that blue shark catch rates were stable in the Atlantic, as well as in the Pacific and Indian Oceans. Assessments of shark status based on fishery catch rates as well as catch data have shown some decline of shortfin mako sharks, but no clear trend for blue sharks in the Atlantic (Babcock and Nakano, 2008). There is evidence of a decline in an eastern Pacific population of common threshers followed by some rebuilding (Smith et al., 2008b). Studies comparing shark catch rates in historical surveys to catch rates from modern commercial fisheries (from observer data) have estimated declines in abundance of more than 90% for oceanic whitetip and silky sharks in the Gulf of Mexico (Baum and Myers, 2004) and 87% for blue sharks in the central Pacific Ocean (Ward and Myers, 2005). For many populations of oceanic sharks, there are no data on trends in abundance or the available data are patchy, unreliable, or contradictory; however, for populations that have been studied, most have shown a declining trend (Camhi, 2008; Camhi et al., 2008a). Thus, the concern that some of the many populations that have never been studied may be depleted seems warranted (Camhi, 2008). One reason for concern about population declines of pelagic sharks is that, because of their life history, sharks are particularly at risk for extinction (Pikitch, 2005). Of 133 marine vertebrate, invertebrate, and algae populations that have gone locally, regionally, or globally extinct within the last 300 years (Dulvy et al., 2003), 64 were marine fishes, of which 32 were sharks and rays. Considering that sharks and rays represent only about 5% of all marine fishes (Nelson, 1994), the fact that half of the extinct populations of fishes were sharks and rays implies that they may be particularly vulnerable. It is also worth noting that habitat loss or ecological impacts of invasive species were the cause (at least in part) of extinction for 25 of the 32 extinct finfish populations, whereas exploitation was the cause of extinction for all 32 of the sharks and rays (Dulvy et al., 2003). Extinction risk was correlated strongly with large body size, and less strongly with small geographic range and habitat specialization. Oceanic sharks are wide-ranging and are not habitat specialists, but they are all large-bodied animals and are heavily exploited, implying that they may indeed be at increased risk. Removal of apex predators has been demonstrated to profoundly impact some marine ecosystems (Estes et al., 1998). As the apex predators of the high seas, pelagic sharks are likely to strongly influence food web structure (Bascompte et al., 2005). The understanding that alterations in food web processes could undermine the sustainability of fisheries

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Sharks of the Open Ocean

and cause undesirable changes in ecosystem structure and function (Bakun and Weeks, 2004) has recently led to a paradigm shift in fisheries management, from a focus on managing each species individually to ecosystem-based fishery management (Pikitch et al., 2004). The large-scale removal of oceanic sharks could have far-ranging negative ecosystem effects. For example, Stevens et al. (2000) used the dynamic mass balance model Ecosim to predict the impacts of shark removals from three ecosystems. In all three systems, the biomass of some prey species increased two- to threefold after shark removal, but other prey species decreased or remained stable and the biomass dynamics were complex and difficult to predict. Similarly, the food web model of Bascompte et al. (2005) implied that sharks strongly influence the functioning of food webs, so that the overfishing of sharks may have contributed to the degradation of Caribbean coral reefs. Thus, overexploitation of oceanic sharks may have consequences for marine ecosystems that are difficult to predict and even more difficult to reverse.

The future of oceanic sharks Oceanic sharks remain among the least studied and least managed of the elasmobranchs, although they are among the most heavily impacted by fishing. Over the past decade, progress has been made in improving our understanding of the biology, status, and trends of oceanic sharks, and in documenting the catches. Management has also improved, but it may be too little and too late. The 1999 FAO International Plan of Action for the Conservation and Management of Sharks (IPOA-Sharks) called on states and regional fishery management organizations to assess the status of shark populations and develop plans for their management. As of this writing, only 22 of 113 shark-fishing states have accomplished either of these tasks (Cavanagh et al., 2008). A more encouraging development is that measures to ban or limit “finning” – the practice of retaining the fins of a shark and discarding the carcass (Meliane, 2003; Camhi et al., 2008b) – have been enacted to varying degrees by Australia, Brazil, Canada, Costa Rica, Ecuador, Egypt, the European Union, Israel, Namibia, Nicaragua, Oman, Palau, Seychelles, South Africa, Spain, and the United States (Fig. 1.2). In 2004, the International Commission on the Conservation of Atlantic Tunas (ICCAT) passed a resolution banning finning by ICCAT member nations in the Atlantic, which was the first finning ban in international waters. Similar resolutions were passed in 2005 by the General Fisheries Commission of the Mediterranean (GFCM), the Inter-American Tropical Tuna Commission (IATTC), the Indian Ocean Tuna Commission (IOTC), and the Northwest Atlantic Fisheries Organization (NAFO), and in 2006 by the Southeast Atlantic Fisheries Organization (SEAFO) (Camhi et al., 2008b). Because oceanic sharks are a major component of the fin trade, these conservation measures may help reduce the mortality of oceanic sharks, and may improve the quality of the data on oceanic shark catches, but only if these measures are adequately enforced. This book provides new information on the biology and ecology of oceanic sharks, their fisheries, and their management, and also serves as a compilation of the current state of knowledge. In gathering this information, we were struck by the many gaps in our knowledge of the oceanic sharks. Although many papers have been published on pelagic sharks, they tend to focus on only a few populations. For example, while many individual

European Union

Canada (Atlantic) United States

NAFO GFCM Egypt

IATTC Costa Rica

Nicaragua

ICCAT

Israel Palau

Oman

Ecuador

Seychelles Brazil IOTC

Australia

SEAFO South Africa

Fig. 1.2 Countries and regional fisheries management organizations that have taken measures to ban or limit finning (Meliane, 2003; Camhi et al., 2008b).

Introduction to Sharks of the Open Ocean

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oceanic sharks have been tagged, the vast majority have been blue sharks in the Northwest Atlantic (Kohler and Turner, 2008). Sharks that are farther offshore and are not caught in recreational fisheries are not as likely to be tagged. Clearly, there is a pressing need for research to assess the status of understudied species like the threshers and silky sharks. Recent improvements in the quality of catch statistics and efforts to infer catches from trade data are laudable, and should be continued. The research presented in this volume, as well as in other studies published in the last several years, makes it clear that oceanic sharks are at risk from high-seas fishing, and that some populations are depleted and perhaps even threatened with extinction. We call on all fishing nations, as well as the regional fishery management organizations, to begin or intensify their efforts to assess the status of these species and to develop and implement effective management plans to ensure sustainable populations of oceanic sharks, before it is too late to stem and reverse the decline of the sharks of the open ocean.

References Au, D. W., Smith, S. E. and Show, C. (2008) Shark productivity and reproductive protection, and a comparison with teleosts. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Babcock, E. A. and Nakano, H. (2008) Data collection, research, and assessment efforts for pelagic sharks by the International Commission for the Conservation of Atlantic Tunas. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Bakun, A. and Weeks, S. J. (2004) Greenhouse gas buildup, sardines, submarine eruptions and the possibility of abrupt degradation of intense marine upwelling ecosystems. Ecology Letters 7, 1015–1023. Bascompte, J., Melián, C. J. and Sala, E. (2005) Interaction strength combinations and the overfishing of a marine food web. Proceedings of the National Academy of Sciences 102, 5443–5447. Baum, J. K. and Myers, R. A. (2004) Shifting baselines and the decline of pelagic sharks in the Gulf of Mexico. Ecology Letters 7, 135–145. Baum, J. K., Myers, R. A., Keller, D. G., Worm, B., Harley, S. J. and Doherty, P. A. (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299, 389–391. Beerkircher, L. R., Cortés, E. and Shivji, M. S. (2008) Case study: Elasmobranch bycatch in the pelagic longline fishery off the southeastern United States, 1992–1997. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Block, B. A., Dewar, H., Blackwell, S. B., Williams, T. D., Prince, E. D., Farwell, C. J., Boustany, A., Teo, S. L. H., Seitz, A., Walli, A. and Fudge, D. (2001) Migratory movements, depth preferences and thermal biology of Atlantic bluefin tuna. Science 293, 1310–1314. Bonfil, R., Meyer, M., Scholl, M. C., Johnson, R., O’Brien, S., Oosthuizen, H., Swanson, S., Kotze, D. and Paterson, M. (2005) Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science 310, 100–103. Boustany, A. M., Davis, S. F., Pyle, P., Anderson, S. D., Le Boeuf, B. J. and Block, B. A. (2002) Expanded niche for white sharks. Nature 415, 35–36. Boustany, A. M., Weng, K. C. M., Anderson, S. D., Pyle, P. and Block, B. A. (2008) Case study: White shark movements in the North Pacific pelagic ecosystem. In: Sharks of the Open Ocean: Biology,

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Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Camhi, M. D. (2008) Conservation status of pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Camhi, M., Fowler, S., Musick, J., Bräutigam, A. and Fordham, S. (1998) Sharks and Their Relatives: Ecology and Conservation. IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, 39 pp. Camhi, M. D., Lauck, E., Pikitch, E. K. and Babcock, E. A. (2008a) A global overview of commercial fisheries for open ocean sharks. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Camhi, M. D., Fordham, S. V. and Fowler, S. L. (2008b) Domestic and international management for pelagic sharks. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Campana, S. E., Joyce, W., Marks, L., Hurley, P., Natanson, L. J., Kohler, N. E., Jensen, C. F., Mello, J. J., Pratt Jr., H. L., Myklevoll, S. and Harley, S. (2008) The rise and fall (again) of the porbeagle shark population in the Northwest Atlantic. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Cavanagh, R. D., Fowler, S. L. and Camhi, M. D. (2008) Pelagic sharks and the FAO International Plan of Action for the Conservation and Management of Sharks. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Clarke, S. (2003) Quantification of the Trade in Shark Fins. Ph.D. thesis, Imperial College London, London, UK, 327 pp. Clarke, S., Magnusson, J. E., Abercrombie, D. L., McAllister, M. and Shivji, M. S. (2006) Identification of shark species composition and proportion in the Hong Kong shark fin market using molecular genetics and trade records. Conservation Biology 20(1), 201–211. Compagno, L. J. V. (2008) Pelagic elasmobranch diversity. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Cortés, E. (2008) Comparative life history and demography of pelagic sharks. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Dulvy, N. K., Sadovy, Y. and Reynolds, J. D. (2003) Extinction vulnerability in marine populations. Fish and Fisheries 4, 25–64. Estes, J. A., Tinker, M. T., Williams, T. M. and Doak, D. F. (1998) Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282, 473–476. Friedlander, A. M. and DeMartini, E. E. (2002) Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian Islands: The effects of fishing down apex predators. Marine Ecology Progress Series 230, 253–264. Grogan, E. D. and Lund, R. (2004) The origin and relationships of early Chondrichthyes. In: Biology of Sharks and Their Relatives (eds. J. C. Carrier, J. A. Musick and M. R. Heithaus). CRC Press, Boca Raton, FL, pp. 3–31. Hazin, F. H. V., Broadhurst, M. K., Amorim, A. F., Arfelli, C. A. and Domingo, A. (2008) Catches of pelagic sharks by subsurface longline fisheries in the South Atlantic Ocean during the last century: A review of available data with emphasis on Uruguay and Brazil. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK.

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Hueter, R. E. and Simpfendorfer, C. A. (2008) Case study: Trends in blue shark abundance in the western North Atlantic as determined by a fishery-independent survey. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Hutchings, J. A. and Reynolds, J. D. (2004) Marine fish population collapses: Consequences for recovery and extinction risk. Bioscience 54, 297–309. Kohler, N. E. and Turner, P. A. (2008) Stock structure of the blue shark (Prionace glauca) in the North Atlantic Ocean based on tagging data. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. McAllister, M. K., Pikitch, E. K. and Babcock, E. A. (2008) Why are Bayesian methods useful for the stock assessment of sharks? In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Meliane, I. (2003) Shark finning. IUCN Information Paper. Marine Programme, IUCN, Malaga, Spain. Myers, R. A. and Worm, B. (2003) Rapid worldwide depletion of predatory fish communities. Nature 423, 280–283. Nakano, H. (1996) Historical CPUE of pelagic shark caught by Japanese longline fishery in the world. Document AC 13.6.1 Annex, information paper submitted to the thirteenth CITES Animals Committee, Prague, Czech Republic, 7 pp. Nelson, J. S. (1994) Fishes of the World, 3rd edn. John Wiley & Sons, New York. Pauly, D. (2005) The sea around us project. www.seaaroundus.org, accessed 30 March 2005. Pikitch, E. K. (2005) The gathering wave of ocean extinctions. In: State of the Wild 2006: A Global Portrait of Wildlife, Wildlands, and Oceans (ed. S. Gynup). Island Press, Washington, DC, pp. 195–201. Pikitch, E. K., Santora, C., Babcock, E. A., Bakun, A., Bonfil, R., Conover, D. O., Dayton, P., Doukakis, P., Fluharty, D., Heneman, B., Houde, E. D., Link, J., Livingston, P., Mangel, M., McAllister, M. K., Pope, J. and Sainsbury, K. J. (2004) Ecosystem-based fishery management. Science 305, 346–347. Priede, I. G., Froese, R., Bailey, D. M., Bergstad, O. A., Collins, M. A., Dyb, J. E., Henriques, C., Jones, E. G. and King, N. (2006) The absence of sharks from abyssal regions of the world’s oceans. Proceedings of the Royal Society of London, Series B 373, 1435–1441. Smale, M. J. (2008) Pelagic shark fisheries in the Indian Ocean. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Smith, S. E., Au, D. W. and Show, C. (2008a) Intrinsic rates of increase in pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Smith, S. E., Rasmussen, R. C., Ramon, D. A. and Cailliet, G. M. (2008b) The biology and ecology of thresher sharks (Alopiidae). In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Snelson Jr., F. F., Roman, B. L. and Burgess, G. H. (2008) The reproductive biology of pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Stevens, J. D., Bonfil, R., Dulvy, N. K. and Walker, P. A. (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57, 476–494. Walker, T. I., Taylor, B. L., Brown, L. P. and Punt, A. E. (2008) Embracing movement and stock structure for assessment of Galeorhinus galeus harvested off southern Australia. In: Sharks of

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the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Ward, P. and Myers, R. A. (2005) Shifts in open-ocean fish communities coinciding with the commencement of commercial fishing. Ecology 86, 835–847. Watson, R., Kitchingman, A., Gelchu, A. and Pauly, D. (2004) Mapping global fisheries: Sharpening our focus. Fish and Fisheries 5, 168–177. Williams, P. G. (1999) Shark and related species catch in tuna fisheries of the tropical western and central Pacific Ocean. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/2. FAO, Rome, Italy, pp. 860–879. Worm, B., Lotze, H. K. and Myers, R. A. (2003) Predator diversity hotspots in the blue ocean. Proceedings of the National Academy of Sciences 100, 9884–9888.

Chapter 2

Pelagic Elasmobranch Diversity Leonard J. V. Compagno

Abstract Pelagic sharks include oceanic and semi-oceanic species of sharks and rays, active freeswimming species that live in the world’s oceanic basins and over the continental and insular slopes and rises. The group is relatively small, comprising about 6% of the world’s total number of cartilaginous fish species. Pelagic sharks show few derived body plans or ecomorphotypes compared to coastal shark species, but have two ecomorphotypes specialized for life in the open ocean (macroceanic and microceanic). They are best represented among the orders Squaliformes, Carcharhiniformes, Lamniformes, and Rajiformes, with a few members of the Hexanchiformes and Orectolobiformes and none from the other shark orders. This chapter presents an annotated checklist and discussion of pelagic sharks, and also considers the impact of human activities on these species. Key words: biodiversity, taxonomy, pelagic sharks, ecomorphotypes, Squaliformes, Carcharhiniformes, Lamniformes, Rajiformes, Hexanchiformes, Orectolobiformes.

Introduction There have been few reviews of the biodiversity of pelagic sharks (Casey et al., 1992). The term “shark” as used here includes the batoids (skates and rays) as well as the true sharks. “Pelagic shark” refers to highly mobile species that are not closely associated with the sea bottom, as opposed to benthic or bottom-dwelling sharks. “Oceanic” species include those pelagic sharks that live their lives in whole or in part in the ocean basins away from continental landmasses, although some of these species come to the edges of the continental and insular shelves (in water about 200 m deep) and may come close inshore over the shelves to feed, breed, or partake in other activities, including social interactions. These oceanic species may be epipelagic, confined to the upper, sunlit level or epipelagic zone of the oceans (from the surface to about 200 m deep); mesopelagic, living in the twilight zone below the epipelagic zone where little light penetrates (from 200 to 1,000 m); or bathypelagic, inhabiting the sunless zone below 1,000 m and extending to the deep slopes, rises, ocean floor, and trenches (down to 6,000 m or more). “Semipelagic” sharks penetrate oceanic waters but concentrate close to continental landmasses over the continental slopes and rises. Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Pelagic shark diversity The diversity of pelagic sharks is very low compared to that of shelf- and slope-dwelling sharks; Compagno (1990) estimated that about 2% of cartilaginous fishes were oceanic. Using the present taxonomical estimate of 1,164 species of cartilaginous fishes, including undescribed and dubious species, a revised estimate of the numbers of oceanic and semipelagic sharks suggests that 2.7% of all living cartilaginous fishes are oceanic, while an additional 2.8% are semipelagic (Table 2.1). The orders Squaliformes and Lamniformes dominate the oceanic group in species diversity, while members of the order Carcharhiniformes probably dominate in biomass. The orders Carcharhiniformes, Rajiformes, and Squaliformes are the most diverse semipelagic sharks. No chimaeras (Chimaeriformes) are oceanic or semipelagic, with most species living on the continental and insular slopes. Compagno (1990) analyzed sharks in terms of ecomorphotypes, which can include diverse taxa that may or may not be phyletically related but are grouped together by similarities in morphology, habitat, and behavior. Oceanic sharks exhibit several of these ecomorphotypes: the high-speed or tachypelagic, tuna-shaped morphotype for members of Lamnidae, such as the porbeagle, salmon shark, and shortfin mako; the archipelagic or modified tachypelagic superpredator morphotype for the white shark (also Lamnidae); the macroceanic morphotype of large oceanic sharks with long pectoral fins, such as the blue shark, oceanic whitetip shark, silky shark, threshers, longfin mako, and megamouth shark; the microceanic morphotype of small- to moderate-sized oceanic sharks with long, fusiform bodies and small pectoral fins, including dwarf members of the Squaliformes and certain members of the Lamniformes such as the crocodile shark; the modified rajobenthic or skatelike rhomboidal form of the pelagic stingray; and the aquilopelagic or eagleray morphotype of oceanic devilrays (Mobulidae). Semipelagic sharks share morphotypes found in slope- and shelf-dwelling cartilaginous fishes, including several types not seen in specialized oceanic sharks. The following survey describes the oceanic and semipelagic sharks, arranged by order and family. General distributional information on these groups is derived in part from

Table 2.1 Number of oceanic and semipelagic shark species among six orders, and as a percentage of all species in the respective orders.* Order

Orectolobiformes Lamniformes Carcharhiniformes Hexanchiformes Squaliformes Rajiformes Total number of species (and % of all cartilaginous species) *

Number of oceanic species 1 11 3 – 9–13 2–3 26–31 (2.2–2.6%)

% of species in order

Number of semipelagic species

2.9 73.3 1.1 – 6.0–8.7 0.3–0.5

– 3 15 2 3–5 8

% of species in order – 20.0 5.3 33.3 2.0–3.3 1.2

31–33 (2.6–2.8%)

Percentages were calculated by dividing the maximum number of oceanic or semipelagic species into the maximum number of species in each order.

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Bigelow and Schroeder (1948, 1953, 1957), Compagno (1984, 1988, 2001, 2002, 2007a, b), Compagno and Niem (1998), Compagno et al. (1995, 1999, 2005), Ebert (1990), Fowler (1941), Garman (1913), Last and Stevens (1994), McEachran and de Carvalho (2002), McEachran and Notarbartolo di Sciara (1995), and Notarbartolo di Sciara (1987), as well as from unpublished database and field report files on chondrichthyan distribution developed by the writer over the past two decades for FAO publications and other work. Order Orectolobiformes: carpet sharks Family Rhincodontidae: whale sharks Rhincodon typus (Smith, 1828). Whale shark. Oceanic, semipelagic, and littoral. Carpet sharks are mostly benthic and inshore species, though some are littoral and more active swimmers (families Stegostomatidae, Ginglymostomatidae). A notable exception among orectoloboids is the whale shark, a pelagic species often found near oceanic islands that feeds on plankton in both coastal and oceanic waters. Its oceanic movements have been studied by conventional tag recoveries and by satellite tracking in the eastern Pacific and Indian Ocean. Order Lamniformes: mackerel sharks Family Mitsukurinidae: goblin sharks Mitsukurina owstoni (Jordan, 1898). Goblin shark. Semipelagic, benthic on continental slopes. Family Odontaspididae: sand tiger sharks Odontaspis ferox (Risso, 1810). Smalltooth sand tiger. Littoral, benthic, and semipelagic, on ridge systems and seamounts far from land. Odontaspis noronhai (Maul, 1955). Bigeye sand tiger. Oceanic and rarely littoral. Family Pseudocarchariidae: crocodile sharks Pseudocarcharias kamoharai (Matsubara, 1936). Crocodile shark. Oceanic and semipelagic. Family Megachasmidae: megamouth sharks Megachasma pelagios (Taylor, Compagno and Struhsaker, 1983). Megamouth shark. Oceanic and semipelagic. Family Alopiidae: thresher sharks Alopias pelagicus (Nakamura, 1935). Pelagic thresher. Oceanic and occasionally littoral. Alopias superciliosus (Lowe, 1839). Bigeye thresher. Oceanic, semipelagic, and occasionally littoral and benthic on the continental slopes. Alopias vulpinus (Bonnaterre, 1788). Thresher shark. Oceanic, semipelagic, and littoral. Family Cetorhinidae: basking sharks Cetorhinus maximus (Gunnerus, 1765). Basking shark. Littoral, semipelagic, and occasionally oceanic.

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Family Lamnidae: mackerel sharks Carcharodon carcharias (Linnaeus, 1758). Great white shark. Oceanic, semipelagic, littoral, and occasionally benthic on the continental slopes. Isurus oxyrinchus (Rafinesque, 1810). Shortfin mako. Oceanic, semipelagic, and littoral where continental shelves are narrow. Isurus paucus (Guitart Manday, 1966). Longfin mako. Oceanic, rarely littoral where continental shelves are narrow. Lamna ditropis (Hubbs and Follett, 1947). Salmon shark. Oceanic, semipelagic, and littoral where continental shelves are narrow. Lamna nasus (Bonnaterre, 1788). Porbeagle shark. Oceanic, semipelagic, and littoral. Although presently a small group compared to their previous diversity in Cretaceous and Cenozoic times, the order Lamniformes has a disproportionate number of species that are oceanic, semipelagic, or wide-ranging in oceanic, shelf, and slope waters. The sand tiger shark family (Odontaspididae) has an apparently oceanic, epipelagic, and possibly mesopelagic large species, Odontaspis noronhai, with a microceanic morphotype. This species also occurs on continental and insular slopes, as does O. ferox, another sand tiger species that may be semipelagic (but that needs confirmation). The goblin shark (Mitsukurinidae) is a slope-dweller that may be semipelagic. The crocodile shark (Pseudocarcharias kamoharai) and the megamouth shark (Megachasma pelagios) are, respectively, microceanic and macroceanic epipelagic species that occasionally are littoral on the continental shelves. As a group the thresher sharks (Alopiidae) are littoral and oceanic (with a macroceanic morphotype), but the bigeye thresher (Alopias superciliosus) is a slope-dweller. The basking shark (Cetorhinus maximus) is usually considered a littoral, continental species, but rare records from oceanic islands (e.g., the Hawaiian Islands) and sight records over the continental slopes or even the ocean basins in the western North Atlantic suggest that this is also a semipelagic and at least occasionally oceanic species. Most of the mackerel sharks (Lamnidae) are both littoral and oceanic, except for the longfin mako (Isurus paucus), which seldom penetrates continental waters. The white shark (Carcharodon carcharias) is usually considered a littoral, continental species like the basking shark, but catches of white sharks in mid-ocean and near oceanic islands and ongoing satellite-tagging and genetic studies demonstrate oceanic movements. The white shark apparently descends to the upper slopes and may have the widest habitat and geographic range of any chondrichthyan. Order Carcharhiniformes: ground sharks Family Triakidae: houndsharks Galeorhinus galeus (Linnaeus, 1758). Tope shark. Littoral and semipelagic. Family Carcharhinidae: requiem sharks Carcharhinus albimarginatus (Rüppell, 1837). Silvertip shark. Littoral and semipelagic. Carcharhinus altimus (Springer, 1950). Bignose shark. Semipelagic and benthic on the upper continental slopes. Carcharhinus brachyurus (Günther, 1870). Bronze whaler. Littoral and semipelagic. Carcharhinus brevipinna (Müller and Henle, 1839). Spinner shark. Littoral and semipelagic. Carcharhinus falciformis (Bibron, 1839). Silky shark. Oceanic and semipelagic.

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Carcharhinus galapagensis (Snodgrass and Heller, 1905). Galapagos shark. Littoral and semipelagic. Carcharhinus leucas (Valenciennes, 1839). Bull shark. Littoral and freshwater, occasionally semipelagic. Carcharhinus limbatus (Valenciennes, 1839). Blacktip shark. Littoral and semipelagic. Carcharhinus longimanus (Poey, 1861). Oceanic whitetip shark. Oceanic and semipelagic. Carcharhinus obscurus (Lesueur, 1818). Dusky shark. Littoral and semipelagic. Carcharhinus plumbeus (Nardo, 1827). Sandbar shark. Littoral and semipelagic. Carcharhinus signatus (Poey, 1868). Night shark. Semipelagic. Galeocerdo cuvier (Peron and Lesueur, 1822). Tiger shark. Littoral and semipelagic. Prionace glauca (Linnaeus, 1758). Blue shark. Oceanic and semipelagic, littoral where continental shelves are narrow. Family Sphyrnidae: hammerhead sharks Sphyrna lewini (Griffith and Smith, 1834). Scalloped hammerhead. Littoral and semipelagic. Sphyrna mokarran (Rüppell, 1837). Great hammerhead. Littoral and semipelagic. Sphyrna zygaena (Linnaeus, 1758). Smooth hammerhead. Littoral and semipelagic. Most carcharhiniform sharks are shelf- or slope-dwellers. Three members of the requiem shark family Carcharhinidae, the blue shark (Prionace glauca), silky shark (Carcharhinus falciformis), and oceanic whitetip shark (C. longimanus), are oceanic species and are perhaps the most important oceanic sharks in terms of biomass. Several species of large carcharhinids, the larger hammerheads (Sphyrnidae), and one species of houndshark – the soupfin or tope shark (Galeorhinus galeus) – are semipelagic as well as littoral, while one of the carcharhinids, the night shark (C. signatus), is more strictly offshore and semipelagic and occurs at or beyond the edge of the continental shelves of the tropical and warm-temperate Atlantic. Order Hexanchiformes: cow and frilled sharks Family Chlamydoselachidae: frilled sharks Chlamydoselachus anguineus (Garman, 1884). Frilled shark. Benthic and semipelagic. Family Hexanchidae: sixgill and sevengill sharks Hexanchus griseus (Bonnaterre, 1788). Bluntnose sixgill shark. Benthic and semipelagic. No known hexanchiform sharks are truly oceanic. The frilled shark (Chlamydoselachus anguineus) is a slope-dweller that can occur well off the bottom and may be semipelagic in some places. The bluntnose sixgill shark (Hexanchus griseus) has an enormous geographic and bathymetric range and occurs off oceanic islands and on ridges and seamounts. It is primarily a shelf- and slope-dweller, but may also be semipelagic. Order Squaliformes: dogfish sharks Family Etmopteridae: lanternsharks Etmopterus gracilispinis (Krefft, 1968). Broadband lanternshark. Benthic and semipelagic.

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Etmopterus pusillus (Lowe, 1839). Smooth lanternshark. Benthic and semipelagic. Miroscyllium sheikoi (Dolganov, 1986). Rasptooth dogfish. Benthic and possibly semipelagic. Trigonognathus kabeyai (Mochizuki and Ohe, 1990). Viper dogfish. Benthic and possibly semipelagic. Family Somniosidae: sleeper sharks Scymnodalatias albicauda (Taniuchi and Garrick, 1986). Whitetail dogfish. Oceanic. Scymnodalatias garricki (Kukuyev and Konovalenko, 1988). Azores dogfish. Possibly oceanic. Scymnodalatias oligodon (Kukuyev and Konovalenko, 1988). Sparsetooth dogfish. Possibly oceanic. Scymnodalatias sherwoodi (Archey, 1921). Sherwood dogfish. Possibly oceanic. Zameus squamulosus (Günther, 1877). Velvet dogfish. Benthic and semipelagic. Family Dalatiidae: kitefin sharks Euprotomicroides zantedeschia (Hulley and Penrith, 1966). Taillight shark. Oceanic and benthic. Euprotomicrus bispinatus (Quoy and Gaimard, 1824). Pygmy shark. Oceanic and benthic. Heteroscymnoides marleyi (Fowler, 1934). Longnose pygmy shark. Oceanic. Isistius brasiliensis (Quoy and Gaimard, 1824). Cookiecutter or cigar shark. Oceanic. Isistius labialis (Meng, Chu and Li, 1985). South China cookiecutter shark. Oceanic. Isistius plutodus (Garrick and Springer, 1964). Largetooth cookiecutter shark. Oceanic and semipelagic. Mollisquama parini (Dolganov, 1984). Pocket shark. Possibly semipelagic. Squaliolus aliae (Teng, 1959). Smalleye pigmy shark. Oceanic. Squaliolus laticaudus (Smith and Radcliffe, 1912). Spined pygmy shark. Oceanic. Most dogfish sharks are slope-dwellers, with some species ranging onto the shelves at higher latitudes. Most known species of the kitefin shark family Dalatiidae are oceanic and include such small microceanic specialists as the cookiecutter sharks (Isistius), the pigmy sharks (Euprotomicrus and Heteroscymnoides), the taillight shark (Euprotomicroides zantedeschia), and the spined pygmy sharks (Squaliolus). Some of these little sharks are mesopelagic and bathypelagic, and may reach the ocean bottom during vertical migrations. The related sleeper shark family Somniosidae consists mostly of slope-dwellers, though some of the giant sleeper sharks (Somniosus, subgenus Somniosus) occur on the continental shelves at high latitudes. At least one somniosid species, Scymnodalatias albicauda, is oceanic and epipelagic, and is caught on pelagic longlines in high latitudes in the Southern Hemisphere; other members of Scymnodalatias may be oceanic, or slopedwellers, or both. A small dalatiid, the pocket shark (Mollisquama parini), was collected on a submarine ridge off northern Chile and may be a slope-dweller or alternatively semipelagic or oceanic. The somniosid Zameus squamulosus is primarily a slope-dweller but is also semipelagic. There are several semipelagic or potentially semipelagic species in the lanternshark family Etmopteridae, which includes Etmopterus gracilispinis and E. pusillus. These are primarily slope-dwelling species that are also semipelagic.

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Order Rajiformes: skates and rays (batoids) Suborder Torpedinoidei: electric rays Family Torpedinidae: torpedo rays Torpedo nobiliana (Bonaparte, 1835). Great, Atlantic, or black torpedo. Benthic, littoral, and semipelagic. Torpedo semipelagica (Parin and Kotlyar, 1985). Semipelagic torpedo. Semipelagic. Suborder Myliobatoidei: stingrays Family Dasyatidae: whiptail stingrays Dasyatis matsubarai (Miyosi, 1939). Pitted stingray. Benthic and semipelagic. Pteroplatytrygon violacea (Bonaparte, 1832). Pelagic stingray. Oceanic and littoral. Family Myliobatidae: eagle rays Aetobatus narinari (Euphrasen, 1790). Spotted eagle ray or bonnetray. Benthic, littoral, and semipelagic. Aetomylaeus vespertilio (Bleeker, 1852). Ornate or reticulate eagle ray. Benthic, littoral, and semipelagic. Myliobatis californicus (Gill, 1865). Bat ray. Benthic, littoral, and semipelagic. Family Mobulidae: devilrays Manta birostris (Walbaum, 1792). Manta. Littoral and oceanic. Mobula japanica (Müller and Henle, 1841). Spinetail devilray. Littoral and semipelagic or oceanic. Mobula mobular (Bonnaterre, 1788). Giant devilray or devil ray. Littoral and semipelagic or oceanic. Mobula tarapacana (Philippi, 1892). Sicklefin devilray. Littoral and semipelagic or oceanic. Most batoids are shelf- or slope-dwellers, and occur on or near the bottom, though some are more active littoral species in coastal waters. The stingray family Dasyatidae has one notable exception, the pelagic stingray (Pteroplatytrygon violacea), which is oceanic, while the pitted stingray (Dasyatis matsubarai) may be semipelagic as well as coastal-benthic. A few torpedo rays (Torpedo spp.: Torpedinidae) and eagle rays (Aetobatus, Aetomylaeus, and Myliobatis: Myliobatidae) may be semipelagic as well as shelf-dwellers, and the torpedinids may also be slope-dwellers. The devilray family Mobulidae has several littoral species, but the manta (Manta birostris) and possibly the sicklefin devilray (Mobula tarapacana) are oceanic as well as littoral; the closely related species M. japanica and M. mobular are large, possibly semipelagic or oceanic species. Smaller species of apparently littoral mobulids are strong swimmers and also could make oceanic excursions.

Pelagic sharks in perspective As with freshwater sharks and rays, the relatively low diversity of living pelagic elasmobranchs and the low numbers of oceanic species suggest that the oceanic realms are rather marginal for cartilaginous fishes as contrasted to the high diversity of oceanic teleost fishes

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and cephalopods (M. Roeleveld, personal communication). The few shark species that penetrate the open ocean are often large macropredators that feed high in the food chain (some carcharhinids and lamnoids), although blue and thresher sharks exploit medium-sized and small pelagic prey. Large filter-feeding sharks and rays include a handful of species in four families (whale, megamouth and basking sharks, and devilrays), but all of these readily penetrate the oceanic zone, and three are among the largest living fishes (whale shark, basking shark, and manta). The larger oceanic macropredatory and filter-feeding sharks generally are strong swimmers. An anomaly among oceanic species is the pelagic stingray, a species that occupies an oceanic habitat with a body form clearly derived from that of benthic stingrays and that feeds on pelagic invertebrates and small fishes. Few oceanic elasmobranchs are of moderate size (the crocodile shark, whitetail dogfish, and pelagic stingray are among the exceptions in the range of 60–150 cm). More oceanic species are large to gigantic (from 2 to nearly 20 m long) or small to dwarf (less than 50 cm), with some oceanic dogfish (pygmy sharks) among the smallest living sharks at less than 30 cm when mature. Some of these dwarf dogfish have unusual morphological adaptations, including luminous glands (taillight sharks) and specialized jaws and lips for removing plugs of flesh from live prey (cookiecutter sharks). Large oceanic macropredatory and filter-feeding sharks and rays have rivals in the large and diverse oceanic teleosts and in oceanic cetaceans that share their epipelagic habitat and overlap in feeding habits, but the large sharks apparently are competitive with them and some even prey on them. Although some oceanic sharks are uncommon to rare, others are rather common, while a few species (blue and silky sharks) are among the most abundant large sharks in the world and are very important as apical predators in the epipelagic zone. Apparently, low species diversity can coexist with success in abundance, ecological impact, and geographic dispersal, at least for the handful of large macropredatory oceanic sharks. The large filter-feeding oceanic and semi-oceanic families combine low species diversity with sufficient abundance to support targeted fisheries (except for the relatively rare megamouth shark) and have a wide geographic range, but some of these utilize feeding grounds in littoral waters. Moderate-sized oceanic species vary from rare to common (crocodile sharks and pelagic stingrays, respectively) but are not at all diverse. This is unlike cartilaginous fishes on the shelves and slopes, which include many moderate-sized species. Dwarf oceanic species are even less diverse than their counterparts in continental waters, and are generally rare to uncommon and sporadically if widely distributed, though cookiecutter sharks and spined pygmy sharks can be locally abundant. Pelagic sharks are best known from the epipelagic zone, with the greatest known diversity and biomass concentrated there. Less is known about the distribution of pelagic sharks in the mesopelagic and bathypelagic zones owing to difficulties in collecting them in deepwater pelagic gear, although electronic tagging is yielding new data on the depth penetration of a few of the larger species. Pelagic sharks capture our interest because of their size (both great and small), accessibility, beauty, and spectacular adaptations to their unusual (for a chondrichthyan) lifestyles. Unfortunately, pelagic sharks, by virtue of their mostly “shallow” distribution in the world’s oceans, are easily accessible to huge fleets of high-technology fishing vessels that scour the open oceans in search of “marine resources.” Large pelagic sharks are commonly targeted for human utilization, but most often are swept up as bycatch in the

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enormous fisheries targeting high-value teleosts and cephalopods. Even the rarer dwarf species and plankton-feeding giants are not exempt from being caught in fishing gear, and all pelagic sharks are subject to the deleterious effects of pollution and habitat modification from human activities. The dramatic impact of high-seas fisheries on pelagic sharks and the spectacular declines in their numbers have raised widespread concern for their long-term survival and for the negative ecological effects of their loss on the functioning of marine ecosystems. However, the more insidious consequences of environmental degradation may hasten the extinction of pelagic sharks despite future regulation or even cessation of direct human predation. At present, bycatch fisheries on pelagic sharks are still largely operating without control, and environmental changes proceed apace. The effects of pollutants and global warming on pelagic sharks are not well understood, but those species that feed high on the food chain (such as soupfin and white sharks) apparently can and do concentrate heavy metals such as mercury, and may do likewise for deleterious organic chemicals. Poisoned, degraded, and largely sharkless seas may be our gift to posterity.

Acknowledgments Special thanks to Merry Camhi for inviting the present work and for having patience during its long gestation period. Thanks also to George Burgess and Elizabeth Babcock for reviewing versions of the manuscript.

References Bigelow, H. B. and Schroeder, W. C. (1948) Sharks. In: Fishes of the Western North Atlantic. Part 1. Lancelets, Cyclostomes, Sharks (eds. A. E. Parr and Y. H. Olsen). Sears Foundation for Marine Research, New Haven, CT, pp. 59–546. Bigelow, H. B. and Schroeder, W. C. (1953) Sawfishes, guitarfishes, skates and rays; and chimaeroids. In: Fishes of the Western North Atlantic. Part 2. Sawfishes, Guitarfishes, Skates, Rays and Chimaeroids (eds. J. Tee-Van et al.). Sears Foundation for Marine Research, New Haven, CT, pp. 1–562. Bigelow, H. B. and Schroeder, W. C. (1957) A study of the sharks of the suborder Squaloidea. Bulletin of the Museum of Comparative Zoology Harvard 117, 1–150. Casey, J. G., Connett, S. M. H., Compagno, L. J. V., Stevens, J. D., Oulton, G. and Cook, S. F. (1992) The status of pelagic elasmobranchs: Concerns and commentary. Chondros 3(4), 3–6. Compagno, L. J. V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. FAO Fisheries Synopsis No. 125, Parts 1 and 2. FAO, Rome, Italy, 655 pp. Compagno, L. J. V. (1988) Sharks of the Order Carcharhiniformes. Princeton University Press, Princeton, NJ (reprinted by Blackburn Press, Caldwell, NJ, 2003). Compagno, L. J. V. (1990) Alternate life history styles of cartilaginous fishes in time and space. Environmental Biology of Fishes 28, 33–75. Compagno, L. J. V. (2001) FAO Species Catalogue for Fishery Purposes. No. 1. Sharks of the World: An Annotated and Illustrated Catalogue of the Shark Species Known to Date. Vol. 2. Bullhead,

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Mackerel and Carpet Sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO, Rome, Italy, 269 pp. Compagno, L. J. V. (2002) Sharks. In: FAO Species Identification Guide for Fishery Purposes. Vol. 1. The Living Marine Resources of the Western Central Pacific (ed. K. E. Carpenter). FAO, Rome, Italy, pp. 357–505. Compagno, L. J. V. (2007a) FAO Species Catalogue for Fishery Purposes. No. 1. Sharks of the World: An Annotated and Illustrated Catalogue of the Shark Species Known to Date. Vol. 1. Hexanchiformes, Squaliformes, Squatiniformes and Pristiophoriformes. FAO, Rome, Italy (in press). Compagno, L. J. V. (2007b) FAO Species Catalogue for Fishery Purposes. No. 1. Sharks of the World: An Annotated and Illustrated Catalogue of the Shark Species Known to Date. Vol. 3. Carcharhiniformes. FAO, Rome, Italy (in press). Compagno, L. J. V. and Niem, V. H. (1998) Sharks. In: FAO Species Identification Guide for Fishery Purposes. Vol. 2. The Living Marine Resources of the Western Central Pacific (eds. K. E. Carpenter and V. H. Niem). FAO, Rome, Italy, pp. 1195–1368. Compagno, L. J. V., Krupp, F. and Schneider, W. (1995) Tiburones. In: Guia FAO para la identificacion de especies para los fines de la pesca. Pacifico Centro-Oriental (Fishing Area 77) (eds. W. Fischer et al.), Vol. 2. FAO, Rome, Italy, pp. 645–741. Compagno, L. J. V., Last, P. R., Seret, B. and de Carvalho, M. R. (1999) Batoid fishes. General remarks, key to families, and list of families and species occurring in the area. In: FAO Species Identification Guide for Fishery Purposes. Vol. 3. The Living Marine Resources of the Western Central Pacific (eds. K. E. Carpenter and V. H. Niem). FAO, Rome, Italy, pp. 1397–1409. Compagno, L. J. V., Dando, M. and Fowler, S. (2005) A Field Guide to the Sharks of the World. HarperCollins, London, UK. Ebert, D. A. (1990) The Taxonomy, Biogeography and Biology of Cow and Frilled Sharks (Chondrichthyes: Hexanchiformes). Ph.D. thesis, Rhodes University, Grahamstown, South Africa, 308 pp. Fowler, H. W. (1941) The fishes of the groups Elasmobranchii, Holocephali, Isospondyli, and Ostariophysi obtained by United States Bureau of Fisheries Steamer “Albatross” in 1907 to 1910, chiefly in the Philippine Islands and adjacent seas. Bulletin of the United States National Museum 13(100), 1–879. Garman, S. (1913) The Plagiostomia. Memoirs of the Museum of Comparative Zoology Harvard 36, 1–515 (reprinted by Benthic Press, Los Angeles, CA, 1997). Last, P. R. and Stevens, J. D. (1994) Sharks and Rays of Australia. CSIRO, Collingwood, Victoria, Australia. McEachran, J. D. and de Carvalho, M. R. (2002) Batoid fishes. In: FAO Species Identification Guide for Fishery Purposes. Vol. 1. The Living Marine Resources of the Western Central Atlantic (ed. K. Carpenter). FAO, Rome, Italy, pp. 508–514. McEachran, J. D. and Notarbartolo di Sciara, G. (1995) Peces batoideos. In: Guia FAO para la identificacion de especies para los fines de la pesca. Pacifico Centro-Oriental (FAO Fishing Area 77) (eds. W. Fischer et al.), Vol. 2, Part 1. Vertebrados. FAO, Rome, Italy, pp. 746–792. Notarbartolo di Sciara, G. (1987) A revisionary study of the genus Mobula Rafinesque, 1810 (Chondrichthyes: Mobulidae) with the description of a new species. Zoological Journal of the Linnean Society of London 91, 1–91.

Chapter 3

The Reproductive Biology of Pelagic Elasmobranchs Franklin F. Snelson Jr., George H. Burgess and Brenda L. Roman

Abstract We review the reproductive biology of 13 species of pelagic elasmobranchs – family Alopiidae: Alopias pelagicus (pelagic thresher), A. superciliosus (bigeye thresher), and A. vulpinus (common thresher); family Lamnidae: Isurus oxyrinchus (shortfin mako), I. paucus (longfin mako), Lamna ditropis (salmon shark), L. nasus (porbeagle), and Carcharodon carcharias (white shark); family Carcharhinidae: Carcharhinus falciformis (silky shark), C. longimanus (oceanic whitetip shark), C. signatus (night shark), and Prionace glauca (blue shark); and family Dasyatidae: Pteroplatytrygon violacea (pelagic stingray). All of these species are viviparous, but they exhibit diverse modes of reproduction. The lamniform sharks of the families Alopiidae and Lamnidae exhibit aplacental viviparity with embryonic oophagy. The requiem sharks, family Carcharhinidae, exhibit placental viviparity. Reproduction in the stingray involves aplacental viviparity with trophonemata. For each species, we summarize information on litter size, birth size, gestation period, reproductive periodicity, age and size at maturity, and development. When known, patterns of geographic variation in these parameters are also discussed. Key words: embryo, fecundity, gestation, maturity, reproduction, litter size, birth size, shark, stingray, Alopiidae, Lamnidae, Carcharhinidae, Dasyatidae.

Introduction Elasmobranchs are threatened globally in large part because life-history traits that have served so admirably over evolutionary time have become serious liabilities in a world where intense fishing pressure and habitat alteration have become commonplace. The reproductive characteristics of elasmobranchs, such as their growth and longevity attributes, make this group of fishes vulnerable to intensifying anthropogenic threats and impacts. Reproduction in elasmobranch fishes is variable in scope and style and is novel in many ways (see Hamlett, 1999; Hamlett and Koob, 1999; Carrier et al., 2004, for recent overviews). In this chapter we review the modes of reproduction and related life-history parameters of 13 species of pelagic sharks and rays. The types of reproduction exhibited Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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represent a cross section of the breadth of innovation encountered within the viviparous elasmobranchs. As is the case for other aspects of elasmobranch biology, knowledge of reproduction is advanced for some species and rudimentary for others.

Methods and definitions The life-history traits discussed in this review are litter size, birth size, gestation period, reproductively related migrations and seasonality, maturity size and age, and embryonic development. We define these terms and briefly describe the usual means by which these characteristics are determined. The possibilities for error arising from these methods are discussed at the end of this chapter. Litter size refers to the number of young produced from a single gestation and is typically based on the number of developing young found in the uteri of pregnant females. Size at birth is generally estimated by noting the sizes of the largest intrauterine fetuses and the smallest free-swimming neonates. However, age and growth data are sometimes used to back-calculate size at birth. The length of gestation is usually estimated from data on embryo and neonate sizes throughout the year. Also, evidence of mating and parturition time, such as bite marks on females and the occurrence of small free-swimmers, is sometimes used to approximate gestation time. The detection of sexual maturity in elasmobranchs is based on varied criteria that differ between the sexes. In males, the detection of sexual maturity is often based on gross examination of the claspers, the modifications of the pelvic fins that serve to transfer sperm to the female. Traits such as the calcification and/or relative length of the claspers and the ability to rotate the claspers medially have been used. In females, the enlargement and differentiation of the reproductive tract, the presence of yolked oocytes in the ovary, and the presence of embryos in the uterus are all characteristics commonly used to determine maturity. The corresponding age at maturity for both males and females is determined from aging of the vertebrae and other hard structures such as spines, which form annual growth rings in many elasmobranch species. These age data are used to create an age and growth curve, from which a maturity age is extrapolated using estimates of maturity size. Unless otherwise noted, all sizes reported in this chapter are total length (TL). Information about embryonic development is obtained from observation of the size, stage, and morphology of eggs and embryos in the maternal reproductive tract. The following section discusses the three modes of reproduction exhibited by pelagic elasmobranchs.

Modes of reproduction We follow the terminology of Hamlett and Koob (1999) in our discussion of reproductive modes. All species treated here are viviparous in that they give birth to living young, although we include a brief description of oviparity for comparison. The method by which the young are nourished during gestation differs among species, and we use this as a system for grouping species into similar reproductive modes.

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Oviparity In oviparous species of elasmobranchs, fertilized eggs are encapsulated in an egg case and deposited in the external environment. All the nutrients that the embryo requires through the course of development are contained within this egg capsule. None of the pelagic species exhibit oviparity.

Aplacental viviparity with oophagy The lamniform sharks (family Alopiidae, genus Alopias; and family Lamnidae, genera Lamna, Isurus, and Carcharodon) all exhibit aplacental viviparity with embryonic oophagy. Only the right ovary is functional (Pratt, 1988; Gilmore, 1993). After the ova are fertilized, they are packaged singly in egg capsules, called blastodisc capsules, in the nidamental gland. These capsules then move into the uterus, where development takes place. In the first phase of gestation, the embryos are nourished by yolk from the yolk sac inside the capsule (the encapsulated or prehatching phase). Once the yolk is depleted, the still relatively small embryos hatch from the capsule, beginning the posthatching phase of development. During this phase the embryos feed on the unfertilized yolked ova (oophagy) that the mother has continued to produce during gestation. The consumption of these nutritive capsules causes the embryonic stomachs to become distended, so that they are often referred to as “yolk stomachs.” Embryos in the posthatching phase may also be nourished by uterine fluids. Toward the end of gestation, the female stops producing nutritive capsules and the late-stage embryos rely on the digestion of yolk in the yolk stomach for energy until birth. As the name implies, there is no placental connection between fetal and maternal systems in these species. White shark reproduction is very poorly understood, but the limited observations available suggest that this species is similar to other lamnid species.

Placental viviparity The requiem sharks (family Carcharhinidae, genera Carcharhinus and Prionace) are all placental viviparous species. Ova ovulated from the single functional ovary pass through a common ostium into the paired oviducts. In the shell (nidamental) glands they are fertilized and wrapped in a thin capsule. These fertilized capsules move into the paired uteri, where development takes place. During early development, the embryos draw nourishment from the yolk stored in the egg. When the yolk supply is exhausted, the empty yolk sac forms a placenta-like connection with the maternal uterine wall, which becomes highly vascularized. This “pseudoplacenta” or yolk sac placenta is unlike a mammalian placenta in derivation, but it functions like a true placenta, providing nutrient and probably gas exchange between the maternal and fetal systems (see Hamlett and Koob, 1999, for a review). The embryos rely on placental nutrition to fuel the latter part of their intrauterine development. The placental connection is broken just before birth and the embryos resorb the remainder of the yolk sac. Newborn young retain only a faint “umbilical” scar.

Aplacental viviparity with trophonemata The details of reproduction in the pelagic stingray, Pteroplatytrygon violacea (also appearing in the literature under the old name Dasyatis violacea), are not well known. What is

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known, however, is in general agreement with the patterns of reproduction and development that have been reported for other species of stingrays (Struhsaker, 1969; Snelson et al., 1988, 1989; Capapé, 1993; Capapé and Zaouali, 1995; Hamlett et al., 1996; Henningsen, 2000). Ova produced in the left ovary pass into the left oviduct and then move through the shell gland, where they are fertilized and collectively wrapped together in a thin egg capsule or membrane. The capsule moves into the left uterus, where development takes place. At some point in early gestation the egg capsule ruptures and disappears, either being voided or resorbed. Early development of the embryos is nourished by yolk stored in the egg. The yolk is fully utilized by the midpoint of gestation and the yolk sac is resorbed. During the latter half of gestation, the wall of the female’s uterus becomes modified with dense fingerlike projections called trophonemata that extend into the lumen of the uterus. Specialized secretory cells on the elongated trophonemata produce a rich nutritious fluid called histotroph or “uterine milk.” The embryos are bathed in this fluid, which they either ingest or passively absorb as the primary source of their nutrition during the latter half of development.

Reproductive trends in pelagic elasmobranchs Despite the methodological limitations of the reproductive study of elasmobranchs and the specific limitations on the study of pelagic species, some general trends in the reproduction of these species can be identified. First, none of the pelagic species exhibit the oviparous mode of reproduction. Obviously, this mode would be unsuitable in an open ocean habitat, as large, yolky eggs would be swept away or would sink to the ocean floor. Second, although there are obvious taxonomic differences among the species studied here, the sharks, at least, exhibit many commonalities in reproduction. In general, elasmobranchs are characterized by low reproductive rates, with typically low fecundity and long gestation periods relative to other fish species (Cortés, 2000, 2004). However, pelagic elasmobranchs differ from coastal elasmobranchs in having slightly larger litters of smaller young. The carcharhinids and the lamniforms each exhibit their largest litter sizes among pelagic species (Prionace glauca and Isurus oxyrinchus, respectively), as well as typically lower birth sizes relative to maximum adult size. Also, though almost all the pelagic species studied here have relatively rapid growth over their lifetime (Brody or von Bertalanffy growth coefficient k ⬎ 0.10), their growth during their first free-swimming year is typically slower than that of coastal species (Branstetter, 1990). The similarities among the pelagic lamniforms and carcharhinids with respect to these traits lend credence to the idea that habitat is a strong selective force on reproduction, and is a better indicator of reproductive characteristics than taxonomic relationship. Thus, the reproductive trends outlined herein may be better understood if we consider the different challenges presented by coastal and pelagic environments. In a coastal habitat, we would expect higher abundance of both food and predators of varying sizes, as compared to in a pelagic habitat, where food availability would be much more scarce and patchy and predator density much lower. In other words, there may be more selective pressure to produce larger, faster-growing young in coastal habitats, where the food resources exist to sustain them and predator avoidance is more important. In the pelagic environment, having larger litters with smaller young may be more appropriate because of limited resources and the necessity of dispersal.

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Because information on the reproduction of the pelagic stingray and its coastal relatives is limited, it is difficult to make such comparisons in this case, but some general differences are clear. For comparative purposes, we group Pteroplatytrygon violacea with its close relatives, the members of the genus Dasyatis, in which the pelagic stingray was once taxonomically grouped. When considered together with Dasyatis species, P. violacea has similar birth size as a percentage of maximum size. However, it has a shorter gestation time (2 months) than that reported for any Dasyatis species. Also, P. violacea has a larger mean litter size (6) and maximum litter size (9–13) than the Dasyatis species. Thus, it is probable that P. violacea has experienced similar selective pressure as the other pelagic elasmobranchs reviewed here, and that this pressure has influenced its reproduction in similar ways, leading it to produce larger litters in a shorter amount of time. In addition, the organically rich uterine fluid observed by Ranzi (1934) may be a related adaptation to faster growth of the embryos.

Reproduction in lamniform sharks Perhaps the most obvious difference in reproduction between the lamniform species and the other pelagic species is that the lamnids exhibit oophagy, or ingestion by embryos of ovulated unfertilized ova. Although the aplacental oophagous strategy is not as prevalent in elasmobranchs as placental viviparity, it is interesting that species representing both reproductive strategies have successfully colonized the pelagic habitat, and their reproductive parameters are in many ways comparable.

Litter size Compared to many of the other species in this review, the alopiids have relatively small litters (Table 3.1). Both the pelagic thresher (Alopias pelagicus) and the bigeye thresher (A. superciliosus) typically have two young per litter, although litters of one, three, and four have been reported for the latter species (Nakamura, 1935; Bass et al., 1975; Guitart Manday, 1975; Moreno and Morón, 1992; Taniuchi, 1997; Liu et al., 1999; Compagno, 2001). In the common thresher (A. vulpinus), litters of two to four appear to be common, but as many as seven in a litter have been reported (Strasburg, 1958; Moreno et al., 1989; Compagno, 2001). The reports of only one fetus in a litter probably are due to premature abortion (Moreno et al., 1989). No correlation between the size of the litter and the size of the mother has been reported for any Alopias species. Litter sizes for the shortfin mako (Isurus oxyrinchus) are higher, ranging from 4 to 25, with most reports in the range of 8–18 (Branstetter, 1981; Stevens, 1983, 2008; Taniuchi, 1997; Mollet et al., 2000). Using data from several studies, Mollet et al. (2000) calculated the mean litter size for this species as 12.5. Maximum litter size may be as large as 25–30, based on one observation of a lamnid litter from the Mediterranean Sea. However, the identification of the species involved is debatable (Sanzo, 1912; Tortonese, 1950; Mollet et al., 2002b). Larger females appear to have larger litters (Mollet et al., 2000). From the few data available for the longfin mako (I. paucus), litters of two, with a single embryo in each uterus, appear to be common (Guitart Manday, 1975; Gilmore, 1983). However,

Table 3.1 Summary of litter size and birth size, as estimated by largest embryos and smallest free-swimming neonates, in 13 species of pelagic elasmobranchs.* Species

Litter size

Birth size (cm) Largest embryos

Smallest free-swimmers

245,86,101,137 2–48,20,21,39,65,70,96,101,141; mean⫽296,141 266,137; 2–645; 3–797

15886 639; 6820; 73101; 9496; 10067; 10659; 13739 11466,137; 155–1599,45,97

13745; 19085 1309; 155–1618,65,96,136 1179,45; 12097; 14525

Lamnidae Isurus oxyrinchus Isurus paucus Lamna ditropis Lamna nasus Carcharodon carcharias

4–1641,49,62,93,131,141; 1814; 25–30(?)95 2–459,60,70,99; 2–832,45 2–545; 4–5100,140 1–69,53,57,81,122,142; mean⫽453,57,81 2–1452; 2–1719; 4–1418; 5–10146; 99; 16–18(?)42

6062; 64131; 7193; 7749 8799; 9270; 9759 7045 64–669,81,105; 7757; 7953 14552; 151146

⬍6333; 65–718,55,103,113 12355 ⬍5010; 70103; 8763; 96100 6853; 749; 76105 12234,83;12926; 13952

2–166,12,15,21,58,107,135,137,141; mean⫽5–7137,141 1–155,7,9,13,62,67,118,121,132,137,141; mean⫽6–85,7,13,118,132,137,141 4–189,21,76,107,117; mean⫽1176 1–62102; 4–757,9,21,37,108,132,137; up to 82110;10–13568; mean⫽26–3737,102,132,135,139,141

67107; 706; 7712; 8021 617; 64132; 75121 5656; 5921; 63117; 65107 45–519,110,132,137

64137; 6512; 70107; 789,21 66121; 7184 6021; 6217; 66107; 67117 35103; 4521

2–994; 4–789; 5–687,114; 9–13148; mean⫽6106

1989; 2494

⬍2590

Carcharhinidae Carcharhinus falciformis Carcharhinus longimanus Carcharhinus signatus Prionace glauca Dasyatidae Pteroplatytrygon violacea *

Size is total length (cm) for sharks and disk width (cm) for the ray. Superscript numbers refer to reference numbers.

Reproductive Biology of Pelagic Elasmobranchs

Alopiidae Alopias pelagicus Alopias superciliosus Alopias vulpinus

29

30

Sharks of the Open Ocean

litters of three (Muñoz-Chápuli, 1984) and four (H. L. Pratt Jr. and J. G. Casey, personal communication, 1988, as cited in Gilmore, 1993) have been reported. Compagno (2001) reported litter sizes ranging from two to eight, probably based on an unconfirmed litter of eight reported by Casey (1986). Both species of Lamna usually have four young per litter, with two embryos per uterus. For the porbeagle (L. nasus), reports range from one to six per litter (Gauld, 1989; Francis and Stevens, 2000; Jensen et al., 2002); the salmon shark (L. ditropis) has litters of two to five embryos (Tanaka, 1980; Nagasawa, 1998; Compagno, 2001). Litter size for the white shark (Carcharodon carcharias), like all aspects of its reproduction, is known from only a few documented records. Documented fecundity ranges from 2 to 14, with an average of about 9 (Bigelow and Schroeder, 1948; Uchida et al., 1987, 1996; Bruce, 1992; Francis, 1996; Malcolm et al., 2001; Mollet, 2004). Some of the smaller brood sizes likely resulted from embryos being aborted prior to examination (Bruce, 2008). A litter that possibly consisted of 16–18 embryos was reported by Cliff et al. (2000), but the exact count is in question.

Birth size Size at birth in Alopias species ranges from 100 to 190 cm TL (Table 3.1). These are relatively large birth sizes for sharks, and the largest among the pelagic species reviewed here. However, the total length measurement in these species is greatly influenced by the long upper lobe of the caudal fin. Most estimates of birth size of A. superciliosus range from 100 to 140 cm (Bass et al., 1975; Gilmore, 1983; Moreno and Morón, 1992; Chen et al., 1997; Compagno, 2001). Although some authors have suggested much smaller birth sizes, from 60 to 75 cm (Nakamura, 1935; Bigelow and Schroeder, 1948; Cadenat, 1956), these lower estimates may be based on premature embryos (Bass et al., 1975) or small sample sizes. Nonetheless, there may be regional differences in birth size for this species, pups being born at larger sizes (135–140 cm) in the Northwest Pacific than in other regions (Chen et al., 1997). The largest embryo recorded for this species was 137 cm (Chen et al., 1997). The smallest captured free-swimming neonate was 130 cm (Bigelow and Schroeder, 1948). The only estimate of birth size for A. pelagicus based on a large sample is 158–190 cm for sharks taken in Taiwanese waters (Liu et al., 1999). However, Compagno (2001) reported a 137-cm free-swimming individual from the western Indian Ocean, suggesting that there may also be regional differences in birth size for this species. Estimates of size at birth in A. vulpinus range from 110 to 160 cm and are comparable throughout its range (Gubanov, 1972; Moreno et al., 1989; Compagno, 2001). Freeswimming young as small as 117–120 cm and term fetuses as large as 159 cm have been reported (Bigelow and Schroeder, 1948; Moreno et al., 1989). Cailliet et al. (1983) estimated size at birth at 158 cm from the von Bertalanffy growth equation. It has been suggested that larger females give birth to larger neonates (Bigelow and Schroeder, 1948; Gubanov, 1978), but Moreno et al. (1989) found no correlation between the maximum embryo size and maternal size. Isurus oxyrinchus has a rather large size at birth, with most estimates ranging from 60 to 70 cm (Bass et al., 1975; Stevens, 1983; Mollet et al., 2000; Compagno, 2001).

Reproductive Biology of Pelagic Elasmobranchs

31

However, embryos may occasionally reach larger sizes. Mollet et al. (2000) reported embryos as large as 71 cm, and Duffy and Francis (2001) observed a litter of eight with sizes ranging up to 77 cm. Free-swimming neonates of this species have been reported as small as 63 cm (Casey and Kohler, 1992). The young of I. paucus are probably born at sizes greater than 90 cm. The largest embryos recorded are 92 cm (Guitart Manday, 1975) and 97 cm (Gilmore, 1983), and the smallest free-swimming individuals reported are 123 and 125 cm (Garrick, 1967). Compagno (2001) suggested birth sizes in the range of 97–120 cm. Estimates of birth size for Lamna nasus are in the range of 68–80 cm, and this appears to hold for both Northern and Southern Hemispheres (Aasen, 1963; Bass et al., 1975; Francis and Stevens, 2000; Jensen et al., 2002). The largest reported embryos were 73–79 cm, and the smallest reported free-swimming neonate was 68 cm (Francis and Stevens, 2000). Reports of large embryos and small free-swimming young of L. ditropis are scanty. Birth size for this species is probably 84–96 cm (Nagasawa, 1998; Goldman, 2002). However, Blagoderov (1994) reported a free-swimming individual less than 50 cm long. Birth size for Carcharodon carcharias is estimated in the range of 120–150 cm (Francis, 1996). The largest embryos reported are 145 cm (New Zealand; Francis, 1996) and 151 cm (Japan; Uchida et al., 1996). The length of the smallest known free-swimming neonate is 122 cm based on three specimens, one taken in the western North Atlantic off New York and the other two taken in the eastern North Pacific off California (Casey and Pratt, 1985; Klimley, 1985). It is interesting that two of these neonates weighed 12 and 16 kg, respectively (Casey and Pratt, 1985), whereas large embryos weighed as much as 26–32 kg (Francis, 1996; Uchida et al., 1996). Perhaps newborn white sharks lose weight initially as they are learning to feed (Francis, 1996). Questionable or erroneous reports of birth size are discussed by Francis (1996).

Gestation period The apparent lack of seasonality in the reproductive cycles of the alopiids makes it difficult to determine the length of their gestation, and so far no direct evidence has been obtained. The best estimate to date of the gestation period for all three Alopias species appears to be Holden’s (1974) calculation of 12 months using the von Bertalanffy growth equation (Table 3.2). Because they captured two pregnant Isurus oxyrinchus females with embryos of significantly different sizes in January off Puerto Rico, Mollet et al. (2000) concluded that gestation in this species must be longer than 1 year. Using a variety of assumptions, they predicted a gestation period of 15–18 months, and possibly as long as 24 months. However, Duffy and Francis (2001) reported a litter from New Zealand waters that was almost 6 months out of phase with the Mollet et al. (2000) seasonal data for embryo size. From the Mollet et al. embryonic growth model, gestation for the largest embryo in this litter would be 21 months. They suggested that the entire reproductive cycle is 3 years, which includes a resting period of about 18 months. The length of gestation is unknown in I. paucus owing to a general lack of knowledge of the biology of the species. The gestation period of Lamna nasus is difficult to estimate because of conflicting reports of reproductive seasonality. A period of 8–9 months has been suggested based on

32

Sharks of the Open Ocean

Table 3.2 Summary of gestation period and resting period in 13 species of pelagic elasmobranchs.* Species

Gestation period (months)

Resting period (months)

Alopiidae Alopias pelagicus Alopias superciliosus Alopias vulpinus

1280 1280 1280

No86 – –

Lamnidae Isurus oxyrinchus Isurus paucus Lamna ditropis Lamna nasus Carcharodon carcharias

⬎12113; 15–1841,93; 2149 – 945,64 82; 8–953,81; ⬎1257; 18–24122 ⬎1293; 1893

1893 – – 3–42,53,81 No52; 1892

Carcharhinidae Carcharhinus falciformis Carcharhinus longimanus Carcharhinus signatus Prionace glauca

11–12107; 1212,15 9–12121; 125,7 12–13107 9139; 9–1277,110; 1899

Yes107; 1215 125 12107 No77,110

Dasyatidae Pteroplatytrygon violacea

2114–116; 2–387

–

*

Superscript numbers refer to reference numbers. A dash indicates no data available.

embryo lengths during given months and estimated embryo growth rates (Aasen, 1963; Francis and Stevens, 2000; Jensen et al., 2002). Some authors have suggested gestation periods of more than a year for this species, citing evidence of two distinct size groups of embryos at some times of year (Shann, 1923; Gauld, 1989). Shann (1923) suggested a gestation period between 18 and 24 months. Using limited information about the timing of mating and parturition, Compagno (2001) and Goldman and Musick (2008) suggested that L. ditropis has a gestation period of about 9 months. It is not known whether females of either Lamna species have any significant resting period during the reproductive cycle; however, Gauld (1989) reported large numbers of mature but nongravid females of L. nasus in catches off Scotland. The gestation period of the white shark is not known with certainty (Francis, 1996). From a variety of observations, the gestation period is assumed to be longer than 12 months and may be closer to 18 months from fertilization to parturition (Mollet et al., 2000; Bruce, 2008).

Reproductive periodicity Like gestation period, the reproductive cycle in alopiids has also not been specifically defined. Adult females of Alopias species carry embryos throughout the year, and embryos are found in varying stages of development at practically any given time (Gubanov, 1972, 1978; Gruber and Compagno, 1981; Chen et al., 1997; Liu et al., 1999). Thus, reproductive seasonality appears to be insignificant, if not nonexistent, for these species, and there appears to be no resting period between pregnancies. There is, however, some evidence for protracted, but perhaps seasonal, periods of parturition in A. superciliosus and A. vulpinus. Gilmore (1993) suggested parturition periods for A. superciliosus in the summer, fall, and winter in the Florida Straits.

Reproductive Biology of Pelagic Elasmobranchs

33

Moreno and Morón (1992) concluded that birth occurs over a protracted period from autumn to winter in the Strait of Gibraltar. Another primary or secondary nursery for this species may exist in nearshore Cuban waters, since many small juveniles and females with full-term litters have been observed there (Guitart Manday, 1975). Cailliet and Bedford (1983) suggested that pupping in A. vulpinus in northeastern Pacific populations occurs annually from March to June. There appears to be a nursery ground in this region in the shallow, warm-temperate coastal waters off southern California (Compagno, 2001). Reproductive seasonality in Isurus oxyrinchus seems to be more or less synchronous in populations from both hemispheres, with parturition from late winter to spring (Pratt and Casey, 1983; Stevens, 1983, 1984a; Cliff et al., 1990; Mollet et al., 2000). Duffy and Francis (2001), however, suggested that birth in New Zealand and Australian waters may occur over a protracted period from winter to summer or possibly even year-round, with a peak in the winter to spring period. Recently fertilized females caught off South Africa in March and June suggest that mating occurs there in autumn, just before ovulation (Cliff et al., 1990; Mollet et al., 2000). The reproductive seasonality of I. paucus is a matter of conjecture. Gilmore (1993) suggested a possible mating area in the northern Gulf of Mexico in April, based on the capture of three ripe males and one large female. Since three of the four pregnant longfin makos reported in the literature were captured in the Gulf of Mexico or near the Florida Straits, it is also possible that this is a parturition or midgestation area for the species (Guitart Manday, 1975; Gilmore, 1983, 1993). Reproduction in Lamna species is likely seasonal, but regional differences may occur. Segregation by both size and sex also appears to play a significant role in the reproductive cycles of both species (Aasen, 1963; Tanaka, 1980; Gauld, 1989; Ellis and Shackley, 1993; Blagoderov, 1994; Nagasawa, 1998; Goldman, 2002). For L. nasus, Bigelow and Schroeder (1948) suggested that parturition in the Northwest Atlantic occurs in summer, but Aasen (1963) and Jensen et al. (2002) both supported a spring parturition period (May to June) in this region. Assuming an 8-month gestation period, mating would then be in autumn (September to October), which would concur with Jensen et al. (2002). On the other hand, in populations studied off Scotland, parturition appears to be in the summer, and mating in the winter (Gauld, 1989). For populations in New Zealand and Australian waters, parturition peaks in winter (June to July), but may extend over a protracted period from April to September (Francis and Stevens, 2000). Thus, reproductive seasonality in the two hemispheres may be out of phase by a few months. The considerable variation in embryo length (up to 14.6 cm) that is often observed within litters of this species (Shann, 1923; Gauld, 1989; Francis and Stevens, 2000; Jensen et al., 2002) suggests that the mating period may be protracted. Both the northwestern and the northeastern Pacific populations of L. ditropis appear to give birth in the spring (Tanaka, 1980; Blagoderov, 1994; Goldman, 2002). In the northwest population at least, birthing is followed by a northerly migration, so that in the summer, the assumed mating season (Blagoderov, 1994), adults are found near the coasts of Kamchatka and Sakhalin. However, Tanaka (1980) suggested that copulation occurs in autumn, not summer. Reproductive periodicity and seasonality of Carcharodon carcharias are unknown. Mollet and Cailliet (2002) have suggested that there is an 18-month resting period after

34

Sharks of the Open Ocean

parturition. This, combined with an 18-month gestation period (Mollet et al., 2000; Bruce, 2008), would result in a 3-year reproductive cycle. However, Francis (1996) suggested that there might be no resting period between litters. Evidence in either case is largely circumstantial and indirect, and the time of mating and early embryonic development are unknown. Pupping probably occurs primarily in spring and summer in mostly temperate waters (Fergusson, 1996; Francis, 1996; Uchida et al., 1996). However, off California, pupping may occur into the autumn (Klimley, 1985).

Age and size at maturity On the basis of clasper morphology (Chen et al., 1997) and structure of the ductus deferens (Moreno and Morón, 1992), estimates of size at first maturity for males of Alopias superciliosus range from 270 to 288 cm (Table 3.3). This size range would correspond to an age at maturation of about 9–10 years (Liu et al., 1998). Size at first maturity in females of this species ranges from 300 to 355 cm, with most estimates between 332 and 341 cm (Stillwell and Casey, 1976; Gruber and Compagno, 1981; Moreno and Morón, 1992; Chen et al., 1997). Using these sizes, Liu et al. (1998) estimated that females mature at 12.3–13.4 years. In contrast, Gruber and Compagno (1981) reported much lower estimates of age at maturity using a modification of the von Bertalanffy growth equation. Although they assumed that maturity occurs at sizes similar to those noted above, they concluded that females mature at 4.5 years and males at 3.5 years of age. Liu et al. (1998) suggested that Gruber and Compagno’s (1981) method was inaccurate. Males of A. pelagicus mature at about 267–276 cm, corresponding to an age of 7.0–8.0 years. Females mature at 282–292 cm, corresponding to an age of 8.0–9.2 years (Liu et al., 1999); however, Compagno (2001) reported a mature female of 264 cm. It is possible that regional differences exist. In A. vulpinus, males reach maturity around 314 cm in the Mediterranean and the Northeast Atlantic (Moreno et al., 1989), and around 333 cm off southern California (Cailliet et al., 1983). Bass et al. (1975) suggested that females mature at about 376 cm. It is possible that regional differences exist in female maturity, since Gubanov (1972) reported pregnant females as small as 260 cm in the northwest Indian Ocean and Gohar and Mazhar (1964) reported a 300-cm pregnant female from the Red Sea. A male maturity size of 314 cm would correspond to about 4–5 years of age, and a female maturity size of 376 cm would correspond to about 6–7 years of age (Cailliet et al., 1983). Recent age and growth studies on A. vulpinus suggest that males mature at 293–311 cm and 4.8 years of age, and females at 303 cm and 5.3 years (Smith et al., 2008b). Estimates of maturity in Isurus oxyrinchus indicate that males reach sexual maturity at a smaller size (180–215 cm) than females (263–293 cm) (Bigelow and Schroeder, 1948; Bass et al., 1975; Gubanov, 1978; Stevens, 1983; Cliff et al., 1990; Mollet et al., 2000). However, from an unsubstantiated observation of a 188-cm female in “post-pregnancy,” Gubanov (1978) asserted that females become sexually mature as small as 180 cm. Age-at-size estimates in this species are unsettled. According to Pratt and Casey (1983), who assumed two pairs of vertebral growth rings per year, females mature at around 7 years and males around 3 years. However, Cailliet et al. (1983), assuming only one pair of vertebral rings per year, suggested that males mature at 7 years of age and, by extrapolation,

Table 3.3 Summary of size and age at maturity in 13 species of pelagic elasmobranchs.* Species

Age at maturity (years)

Size at maturity (cm) Female

Male

Female

Alopiidae Alopias pelagicus Alopias superciliosus Alopias vulpinus

267–27645,86 270–28839,96; 290–300136 293–311126; 31497; 3198; 4279

26445; 282–29286 30067; 332–34139,59,96; 35065,136; 3669 26066; 30062; 303126; 315137; 3768; 4279

7–886 3.565; 9–1085 4–525,126

8–9.286 5–665; 12.3–13.485 5.3126; 6–725

Lamnidae Isurus oxyrinchus Isurus paucus Lamna ditropis Lamna nasus Carcharodon carcharias

18067; 1839; 194–2068,41,131 24545 15863; 177100; 186140 150–2001; 16550; 186–20781 304–3398; 379112; 4429; 45734

18067; 26393; 26641; 280131 24545,69 20563; 211–223100,140 1529; 185–20253; 200–2501; 22457; 236–24981 4458; 4509; 450–50052; 45734

3113; 725 – 3–563,140 3–61; 8105 8–10149; 9–1026; 10–1388

7113; 13–1425 – 6–963; 8–10140 6–91; 13105 9–1026; 12–13149; 18–2388

18011; 200132; 210–22512,15,21,135; 239133; 251107 168–196121; 180–1909,84; 1987 15421; 1573; 185–19076 130–160102; 190–19875,78; 218–22077,110; 222–250132

18011; 200132; 210–220133,135,137; ⬎22515; 232–2456,12; 25021; 273107 175–189121; 180–1907,9,84; 2005,67,132; 21421 1653; 17821; 200–20576; 225107 140–160102; 180–20068,75,130,139; 195–24021; 204–208108,137; 213–2449; 220–2227,37,110; 232135; 241132

6–715; 1012

7–915; ⬎1212

4–5121; 6–884 8119 4–5102; 6–725

4–5121; 6–884 10119 5–6102; 6–725

35–4094; 37144; 40–50148

40–5094,148

2–394

2–394

Carcharhinidae Carcharhinus falciformis Carcharhinus longimanus Carcharhinus signatus Prionace glauca Dasyatidae Pteroplatytrygon violacea *

Size is total length (cm) for sharks and disk width (cm) for the ray. Superscript numbers refer to reference numbers. A dash indicates no data available.

Reproductive Biology of Pelagic Elasmobranchs

Male

35

36

Sharks of the Open Ocean

females mature at 13–14 years. Preliminary data from Campana et al. (2002) and from ongoing age and growth studies on the shortfin mako suggest that Cailliet et al.’s assumption is correct (L. Natanson, personal communication). The smallest reported adults of I. paucus are 245 cm for both sexes (Guitart Manday, 1966; Compagno, 2001). There are no other data relevant to the size or age at maturity in this species. For Lamna nasus, the onset of sexual maturity appears to occur at a similar size in both sexes, but estimates of size at maturity are highly variable. Based on varied criteria in different populations, estimates of male maturity size are 150–200 cm (Aasen, 1961), 165 cm (Ellis and Shackley, 1993), and 186–207 cm (Jensen et al., 2002). This size range corresponds to an age at maturation of about 8 years (Natanson et al., 2002). Estimates of maturity size for females are more variable. For the North Atlantic population, estimates are 200–250 cm (Aasen, 1961) and 236–259 cm (Jensen et al., 2002). In Australian and New Zealand waters, female maturity probably occurs at 185–202 cm, suggesting regional differences (Francis and Stevens, 2000; Francis et al., 2008). Bigelow and Schroeder (1948) reported pregnant females of L. nasus as small as 5 ft (152 cm), but no specific observations were reported so the significance of this outlier cannot be assessed. Assuming a maturity size of 236 cm, females mature at around 13 years of age (Natanson et al., 2002). Because reproduction in L. ditropis is poorly known, there are few estimates of maturity. Studies in the northwestern Pacific suggest that males mature at 177–186 cm and 5 years of age, and females at 200–223 cm and 8–10 years of age (Tanaka, 1980; Nagasawa, 1998). In the northeastern Pacific, males mature at 158 cm and 3–5 years, and females at 205 cm and 6–9 years, indicating faster growth in these populations (Goldman, 2002). Estimates of size and age at maturity for the white shark vary widely and differ between males and females (Bruce, 2008). Males probably first reach sexual maturity somewhere between 300 and 400 cm, with most estimates falling in the range of 340–380 cm (Bass et al., 1975; Pratt, 1996; Malcolm et al., 2001). On the basis of a limited number of studies on age and growth, males in this size range would be 7–10 years old (Cailliet et al., 1985; Wintner and Cliff, 1999; Malcolm et al., 2001). Females probably mature somewhere between 450 and 500 cm (Francis, 1996) and 12–18 years of age (Cailliet et al., 1985; Wintner and Cliff, 1999; Malcolm et al., 2001). Several reports of mature females smaller than 430 cm are probably erroneous, and Paterson’s (1986) report of a pregnant 320-cm female is highly unlikely (Francis, 1996).

Development As described in the Introduction, all the lamniform species demonstrate aplacental viviparity and embryonic oophagy. Because embryonic development has been well studied in Lamna nasus, we use it here to illustrate the general pattern of development in the other lamniform sharks. Encapsulated embryos up to about 4 cm long are nourished by yolk from the yolk sac (Jensen et al., 2002). By the time of hatching, at about 3.2 cm, the yolk sac has been almost completely absorbed. At this point, the embryos have not begun feeding on nutritive egg capsules because they do not yet have teeth capable of tearing them open. Prehatching embryos also have external gills (Francis and Stevens, 2000; Jensen et al.,

Reproductive Biology of Pelagic Elasmobranchs

37

2002), which may be the means by which lamnoid embryos absorb yolk from the yolk sac (Mollet et al., 2000). At about 12–15 cm, the embryonic teeth begin to develop, including two relatively large fangs on the lower jaw but only one functional tooth on each side of the upper jaw. Once these teeth develop, the embryos begin to practice oophagy and the external gills are resorbed (Francis and Stevens, 2000). Oophagy peaks in embryos between 26 and 40 cm (Francis and Stevens, 2000; Jensen et al., 2002). As large numbers of egg capsules are consumed, the yolk stomach weight may reach up to 81% of the embryo’s total weight (Templeman, 1966). Toward the end of gestation (at 41–46 cm), the embryonic teeth are shed and embryos probably rely on yolk stored in the stomach. It is likely that females cease ovulation at this time (Francis and Stevens, 2000). In the embryos, the adult teeth probably do not become erect and functional until some time immediately before or after parturition. There is no evidence of adelphophagy (cannibalism of sibling embryos within the uterus) in any of the lamniform species reviewed here, and the lack of erect functional teeth makes embryophagy unlikely. Francis and Stevens (2000) noted one porbeagle embryo that had nonlethal lacerations on its body, probably incurred from a sibling searching for egg capsules in utero. Accordingly, they suggested that this may be the mechanism by which adelphophagy evolved in the sand tiger shark, Carcharias taurus, a related coastal species (Gilmore et al., 1983). Also, if the aggregate blastodiscs observed by Jensen et al. (2002) indeed contain embryos that do not fully develop, it is possible that these encapsulated embryos may be consumed by the more advanced posthatch embryos during the oophagous phase of development. If so, this would be a novel form of intrauterine cannibalism. Early development in Carcharodon carcharias has not been described. With the re-identification of a 36-cm embryo reported to be a white shark as a shortfin mako (Mollet et al., 2002b), the smallest documented embryonic white shark is approximately 100 cm (estimated from photographs) (Uchida et al., 1987, 1996). Although the general developmental pattern described here for L. nasus may apply to C. carcharias as well, the only thing that is known with certainty is that the latter exhibits aplacental viviparity with oophagy (Uchida et al., 1987, 1996; Fergusson, 1996; Francis, 1996; Bruce, 2008). Although three term embryos had teeth and dermal denticles in their stomachs, embryophagy seems unlikely (Francis, 1996; Uchida et al., 1996).

Reproduction in requiem sharks Reproduction in carcharhinid species differs from that in the other reviewed species by the presence of a placental connection between the maternal and fetal systems during some phase of gestation. In fact, of about 43 species of carcharhinid sharks, only the tiger shark, Galeocerdo cuvier, is aplacental (Compagno, 1988). However, even with a different reproductive mode, the placental species discussed in this section exhibit some marked similarities in reproductive traits with the aplacental pelagic species.

Litter size Litter sizes in pelagic requiem sharks fall into two groups. The three species of Carcharhinus have relatively small litters, ranging from 1 to 18 young per brood (Table 3.1).

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Prionace glauca, in contrast, has much larger litters, ranging in size from 4 to 135. Reports of abnormally small litters, such as 1 or 2 in Carcharhinus species and 4 in the blue shark, may be due to counting young that remained after part of the litter had been aborted, as often happens when pregnant elasmobranchs are boated or handled (Bonfil et al., 1993). The little information available suggests that litter size is positively correlated with female size in these species – larger females tend to have larger broods. The oceanic whitetip shark, C. longimanus, has a reported range of litter sizes from 1 to 15. Most reports are in the range of 4–9, with means of about 6–8 (Backus et al., 1956; Strasburg, 1958; Stevens, 1984a; Bonfil et al., 2008). Gohar and Mazhar (1964) reported a range of 10–15 from the Red Sea, and brood sizes may be slightly larger in some parts of the Pacific Ocean (Saika and Yoshimura, 1985; Seki et al., 1998). The silky shark, C. falciformis, has a litter range of 2–16 (Bonfil et al., 1993; Bonfil, 2008), and its mean brood size is about 5–7 (Strasburg, 1958; Taniuchi, 1997). Brood size reports for the night shark, C. signatus, range from 4 to 18 (Bigelow and Schroeder, 1948; Osorno, 1992). Where adequate data are available, the mean litter size in this species is about 11 (Hazin et al., 2000a). The blue shark, Prionace glauca, has by far the largest litters and the greatest range of reported litter sizes (4–135) of the four requiem species considered here. If both the smallest and largest reported litters are discounted as artifactual or unusual, then litters in the range of 25 to 50 are normal. In studies based on large numbers of pregnant females, mean brood size has ranged from 26 to 56 (Gubanov and Grigor’yev, 1975; Stevens, 1984a; Stevens and McLoughlin, 1991; Nakano, 1994; Castro and Mejuto, 1995).

Birth size Estimates of birth size in pelagic carcharhinids range from about 35 to 85 cm TL and fall into two groups. Blue sharks, which produce larger broods, are smaller at birth than the three species of Carcharhinus, which produce fewer young that are larger at birth (Table 3.1). In the blue shark, young are born between 35 and 50 cm (Pratt, 1979; Cailliet and Bedford, 1983; Compagno, 1984; Stevens, 1984a; Castro and Mejuto, 1995). The smallest reported sizes for free-living neonates range from 34 to 53 cm (summarized by Cailliet and Bedford, 1983; Nakano and Nagasawa, 1996). The size at birth estimated from growth equations is 43–44 cm. In the three Carcharhinus species considered here, birth sizes range from 55 to 85 cm. Reports for C. longimanus range from 55 to 77 cm, with most estimates falling in the range of 60–70 cm (Bigelow and Schroeder, 1948; Bass et al., 1973; Compagno, 1984; Seki et al., 1998; Lessa et al., 1999; Bonfil et al., 2008). Seki et al. (1998) examined embryos as large as 75 cm, and free-swimmers as small as 66 cm. For C. signatus, birth size ranges from 60 to 65 cm (Raschi et al., 1982; Compagno, 1984; Garrick, 1985; Osorno, 1992). Raschi et al. (1982) reported embryos as large as 63 cm and free-swimmers as small as 67 cm. Branstetter and McEachran (1986) examined three free-swimming juveniles that were 62–80 cm with umbilical scars still visible. The average size of late-term embryos examined by Osorno (1992) was 61 cm. Carcharhinus falciformis may produce the largest young of the pelagic requiem species, with birth sizes from 64 to 78 cm (Bass et al., 1973; Yoshimura and Kawasaki, 1985; Bonfil et al., 1993). Osorno (1992) reported free-living neonates from 70 to 87 cm; however, Yoshimura and Kawasaki (1985) reported neonates

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as small as 64 cm. Bonfil (2008) suggested that there are regional differences in silky shark size at birth.

Gestation period All estimates of gestation period for these species are 9–13 months, or roughly 1 year (Table 3.2). These estimates are fairly robust for the blue shark (Suda, 1953; Pratt, 1979; Hazin et al., 2000b) and silky shark (Branstetter, 1987; Osorno, 1992; Bonfil et al., 1993), but less firm for the oceanic whitetip (Backus et al., 1956; Seki et al., 1998). The sole estimate for gestation period in the night shark is 12–13 months (Osorno, 1992). The only estimate that is not consistent with the majority is 18 months for the blue shark (Muñoz-Chápuli, 1984).

Reproductive periodicity It is widely held that in many large viviparous sharks, females do not reproduce every year (Backus et al., 1956; Springer, 1960; Clark and von Schmidt, 1965; Branstetter, 1981). Thus, a female may carry young for about 12 months of gestation, then have a “resting” year before ovulating a new batch of eggs and beginning the gestation of a new litter (Table 3.2). This would result in a 2-year cycle for an individual female. Data to support a biannual cycle are difficult to collect, especially when females in different reproductive stages may occur in different geographic zones or undergo extensive migrations. There is some evidence to support a 2-year reproductive cycle in C. falciformis (Branstetter, 1987; Osorno, 1992; Bonfil, 2008), C. longimanus (Backus et al., 1956; Seki et al., 1998), and C. signatus (Osorno, 1992). Pratt’s (1979) data suggest that the blue shark has annual reproduction, without an intervening resting year, and there seems to be no strong contradictory evidence (Hazin et al., 1994; Nakano and Stevens, 2008).

Age and size at maturity For the silky shark, most estimates of size at maturity in females range from 200 to 260 cm, and for males from 210 to 250 cm (Strasburg, 1958; Bane, 1966; Stevens, 1984a, b; Branstetter, 1987; Stevens and McLoughlin, 1991; Bonfil et al., 1993; Bonfil, 2008) (Table 3.3). There is evidence of marked geographic variation in size at maturation. For example, in the eastern Pacific, silky sharks of both sexes may mature at sizes as small as 180 cm (Bonfil, 2008). Two estimates for age at maturity in this species, both based on studies in the Gulf of Mexico, reached different conclusions. Branstetter (1987) estimated age at maturity as 6–7 years for males and 7–9 years for females. In contrast, Bonfil et al. (1993) estimated maturation at 10 years for males and 12⫹ years for females. For the oceanic whitetip shark, most estimates for male size at maturity are 175–190 cm. The literature suggests that females become sexually mature at a slightly larger size, somewhere between 170 and 220 cm (Backus et al., 1956; Bass et al., 1973; Cadenat and Blache, 1981; Seki et al., 1998). Seki et al. (1998) estimated that both males and females in the central Pacific mature at 4 or 5 years. In the southwestern equatorial Atlantic, estimated age at maturation in both sexes is 6–7 years (Lessa et al., 1999).

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There is very little published information on the size at maturation in the night shark. Branstetter and McEachran (1986) noted that a male of 161 cm and two females, 171 and 226 cm TL, were not mature. Amorim et al. (1998) stated that males and females mature at 157 and 165 cm, respectively, but it is not clear how they evaluated sexual maturity. The most extensive data indicate maturation for males at 185–190 cm and for females at about 200 cm (Hazin et al., 2000a). However, Cadenat and Blache (1981) examined pregnant females that were 178–179 cm. From samples taken off northeastern Brazil, the age at sexual maturation in the night shark is estimated to be 8 years for males and 10 years for females (Santana and Lessa, 2004). Most males of the blue shark become sexually mature at about 220 cm, and females become sexually mature at between 200 and 220 cm (Pratt, 1979; Hazin et al., 1994, 2000a; Castro and Mejuto, 1995; Henderson et al., 2001), although Stevens (1974) reported a mature female of 180 cm. Cailliet et al. (1983) estimated age at maturation for both sexes to be 6–7 years. The only noteworthy departure from this estimate is based on a von Bertalanffy growth equation analysis that estimated male maturation at 4–5 years (Nakano, 1994).

Development There have been no detailed studies of development in any of the four carcharhinid species. However, the general pattern of development can be summarized from limited data on these species and from the more detailed analysis of other large carcharhinid sharks (Springer, 1960; Castro, 1993, 1996). Females have a single functional ovary on the right side, with a common ostium opening into paired left and right reproductive tracts. Ovulated ova are fertilized by stored sperm as they pass through the shell (nidamental) gland. A thin, diaphanous egg capsule is deposited around the egg, and it passes into the uterus, where development occurs. During the early part of gestation, the young rely on yolk provisioned in the egg for nutrition. In some cases, the young may also derive nourishment from histotroph (uterine milk) secreted by the female’s uterus and absorbed by the embryo through elongated external gill filaments (Hamlett et al., 1985). Later in gestation, when the yolk is depleted, the embryonic yolk sac develops into a yolk sac placenta that lies in contact with a highly vascularized attachment site on the wall of the female’s uterus. Since the external gill filaments of the embryo are resorbed during midgestation, it is believed that the embryo relies entirely on nutrient exchange via the placenta to sustain later stages of development. It is generally assumed that all of the pups in a litter are born in relatively quick succession, with the birth of the entire litter spanning a few days at most. Individual pups would vary slightly in size at birth depending on the length of gestation and intrauterine growth rate. The hypothesis that blue shark litters are born in “five or six stages” (Gubanov and Grigor’yev, 1975) seems unlikely. The placentation of the silky shark and the blue shark has been described (Gilbert and Schlernitzauer, 1966; Otake and Mizue, 1985). In the silky shark, the placenta is classified as a discoidal type and lacks appendiculae along the yolk sac stalk (also termed the umbilical cord). Both C. longimanus and P. glauca appear to have placentation similar to that of the silky shark (Otake and Mizue, 1985; Compagno, 1988). According to Hamlett and Koob (1999), in most carcharhinid sharks the egg envelope persists throughout gestation

Reproductive Biology of Pelagic Elasmobranchs

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and becomes an integral part of the placenta. However, in the blue shark the egg capsule disappears at some point before the placenta is fully developed (Otake and Mizue, 1985).

Reproduction in the pelagic stingray The pelagic stingray, Pteroplatytrygon violacea, is the only batoid species that can be considered truly pelagic. Its reproductive strategy is distinct from those of the other species reviewed in this chapter, at least at the physiological level. However, comparison of the stingray’s reproductive parameters reveals similarities that may be attributable to habitat influences.

Litter size Only the left ovary and uterus of this species are functional, which is characteristic of most if not all species of the family Dasyatidae. Normal litter size has been reported to range from four to nine (Mollet, 2002a; Mollet et al., 2002a; Neer, 2008) (Table 3.1). Some authors have reported smaller litters (Wilson and Beckett, 1970; Mollet, 2002a), but these cases may represent abnormal events, associated with either premature abortion by stressed females or anomalies of reproduction in captivity. In contrast, Wilson and Beckett (1970) reported one intrauterine egg capsule that contained 13 nonembryonated “egg segments,” though it is unlikely that all of these eggs would have produced term embryos. Capapé (1985) noted that the number of encapsulated eggs is often greater than the number of term embryos in live-bearing rays.

Birth size A broad range of birth sizes, measured as the width of the body or disk from one “wing tip” to the other, have been reported for P. violacea (Table 3.1). Some of this variation may be due to artifacts mentioned in the Introduction. Mean disk widths (DW) of young at birth range from 14 to 24 cm (Mollet, 2002a; Mollet et al., 2002a). Mollet (2002b) reported that neonates smaller than 25 cm DW are taken between September and April in the eastern Pacific off Central America. From this observation, the size at birth is probably in the upper part of the range noted above. Similarly, birth weights show a broad range of variation, both within and between broods (Mollet, 2002a; Mollet et al., 2002a). It is likely that “normal” birth weight is on the order of 200–250 g. Thus, disk width at birth in P. violacea is similar to that in the southern stingray (Dasyatis americana), but birth weight is about 50% less (Henningsen, 2000).

Gestation period All references to the length of gestation in the pelagic stingray refer back to early literature based on studies in the Mediterranean area (Lo Bianco, 1909; Ranzi, 1932; Ranzi and Zezza, 1936). These studies, although not definitive, suggest a gestation period of 2–3 months (Table 3.2). A 2-month gestation cycle would be the shortest recorded for any

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elasmobranch species. A 3-month gestation would be similar to that of Dasyatis sabina (Snelson et al., 1988; Johnson and Snelson, 1996). Other stingrays may have longer gestation periods (Capapé, 1993; Henningsen, 2000). Some rays with unusually long gestation have been shown to have a period of embryonic diapause, resulting in delayed development (Snelson et al., 1989; Villavicencio-Garayzar, 1993; Morris, 1999). There is no information suggesting that P. violacea exhibits developmental diapause.

Reproductive periodicity The reproductive period for the pelagic stingray is poorly understood and may vary geographically. The results from a large data set accumulated for the eastern Pacific population indicate that the rays reproduce in the winter in warm water off the coast of Central America, after which they migrate northward to the southern California coast (Mollet, 2002b). Observations from the western and central Pacific are less clear, but suggest parturition in warmer waters near the equator from November to May. In contrast, Wilson and Beckett (1970) suggested that parturition occurred in August or September in relatively cool waters in the Grand Banks area in the western North Atlantic. Data for the Mediterranean Sea suggest that the rays reproduce in relatively cool waters in the Bay of Naples in July and August. During this time, females were found carrying embryos in various stages of development, suggesting a general lack of synchrony in mating events (Lo Bianco, 1909; Ranzi, 1932). There is no evidence that an individual female reproduces more than once a year, and annual reproduction is a reasonable assumption based on what is known about related species. It is possible that females might produce two clutches of ova per year in captivity (Mollet et al., 2002a). On the basis of what is known about other rays, we suspect that most females reproduce every year, without a “year off ” resting period (Snelson et al., 1988, 1989; Capapé and Zaouali, 1995; Henningsen, 2000).

Age and size at maturity Males reach sexual maturity between 37 and 50 cm DW at an estimated age of 2 years (Table 3.3). Females reach sexual maturity at a similar size, 40–50 cm DW, at about 3 years (Wilson and Beckett, 1970; Tortonese, 1976; Mollet et al., 2002a). The largest male recorded was a captive specimen that reached 68 cm DW and 12 kg at an estimated age of 6–7 years. The largest female on record, also a captive specimen, was 96 cm DW and 46 kg, with an estimated age of 7–8 years (Mollet et al., 2002a). The largest female captured in nature was 80 cm DW (Wilson and Beckett, 1970). Growth models predict a maximum age of 10 years (Mollet and Cailliet, 2002; Mollet et al., 2002a). The maximum age determined from vertebral banding was also 10 years (Neer, 2008).

Development The little that is known about development in this species is consistent with the general pattern of aplacental viviparity with trophonemata characteristic of other stingrays. Intrauterine egg capsules containing several ova weighing 1–2 g each have been noted in both captive and field observations of the pelagic stingray (Lo Bianco, 1909; Ranzi,

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1932, 1934; Wilson and Beckett, 1970; Mollet, 2002a; Mollet et al., 2002a; Neer, 2008). As with other species of stingrays, the diaphanous egg capsule disappears early in gestation, after which the young are free in the uterus. This occurs at about 11 mm DW in P. violacea (Lo Bianco, 1909). At this size, the embryos have long external gill filaments and a large external yolk sac, and the pectoral fins are not fused with the head (Lo Bianco, 1909; Cavaliere, 1955). Four aborted near-term embryos ranged from 117 to 157 mm DW and from 91 to 120 g. They were fully pigmented and had well-formed tail barbs (H. F. Mollet, personal communication; Mollet, 2002a; Mollet et al., 2002a). One anomaly reported for this species that is not characteristic of other stingrays is the wide range of sizes and developmental stages among the young in a single brood (Mollet et al., 2002a). Since most of these observations are based on captive individuals, they may be anomalies associated with stress, nutritional deficiencies, or other artifacts of captivity.

Discussion With the exception of the pelagic stingray, which has been the subject of limited captive study, data on the reproduction of pelagic species are based on examination of wild-caught specimens. Since these animals are large and difficult to handle, studies are often based on relatively few specimens. These limited data are usually collected in different parts of the world’s oceans at different seasons, and interpretation is often based on extrapolation and untested assumptions. Given these limitations, the published literature on reproduction in these species often reflects a broad range of variation and may even lead to different conclusions, some of which may reveal real differences within or between populations, others of which may be artifactual. Some variation in litter size may be related to differences between individual females or to differences between geographically or genetically distinct populations of the same species. Other reported variation may be due to artifacts. Live-bearing elasmobranchs are notorious for aborting pups, especially if they are in advanced stages of development, when the pregnant females are hooked, boated, handled, or otherwise stressed. Thus some reports of unusually small litter sizes probably represent only partial litters. Likewise, there probably is “real” variation in birth size among individual females and distinct populations. In addition, there is size variation among individuals within a single brood of young that were all fertilized at about the same time. However, some data reported in the literature are undoubtedly based on the artifact of premature abortion of developmentally advanced embryos. Shark and ray embryos that appear to be “full term” in development may not necessarily represent the size at which they would have been born naturally. Finally, in some cases, birth size is estimated indirectly by back-calculation using equations employed in age and growth models. Such estimates are based on varied assumptions and may not agree with estimates derived from measurements of embryos or newborn young. Determining the length of gestation is dependent on knowing the times of fertilization of the ova and parturition. The timing of fertilization is estimated from the appearance of fertilized ova or embryos in early stages of development in the uterus. However, the earliest cleavage stages of fertilized ova are not easily recognized without specialized techniques (Simpfendorfer, 1992; Morris, 1999), nor is the timing of mating necessarily

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coincident with the time of fertilization. In many shark species, females mate immediately after giving birth to young, but store sperm for up to 12 months before ovulating and fertilizing a second batch of eggs (Pratt, 1979). The timing of birth is estimated based on the occurrence of large “full-term” embryos and/or the appearance of small free-living neonates, with the same limitations noted earlier. Finally, the length of gestation is likely influenced by the speed of development, which may vary with water temperature or other environmental parameters. Given these limitations, the length of gestation reported for various elasmobranchs varies widely. A significant degree of variation in maturity sizes is also common. For males, clasper development and testicular maturation are not synchronous in some cases, and histological examination of the gonad and reproductive tract is more definitive (Pratt, 1979, 1996). In some maturing females, virgins may first mate as much as 12 months before they ovulate eggs and begin to carry young. The presence of enlarged yolked eggs in the ovary is suggestive of maturity, but only the presence of fertilized ova or developing embryos in the uterus is definitive. Evaluating the attainment of sexual maturity in females is further complicated if there is a resting period in a multiyear cycle, or if there is extensive migration or geographic segregation of females in different stages of reproduction. Furthermore, not all individuals of a species will necessarily become sexually mature at the same chronological age, and all individuals of the same age may not be the same size owing to growth rate differences. Finally, in some wide-ranging species, the size and age at which sexual maturity is achieved may vary geographically. Estimating the age at which sexual maturity is attained is dependent on accurate aging techniques. In the case of pelagic species, vertebrae have been the only structures used to reveal growth rings. It is usually assumed that a pair of growth rings is laid down annually, although there may be exceptions. Despite the wide use of vertebral aging in elasmobranch research, there have been relatively few verification studies, though there is an extensive literature on the details and limitations of vertebral aging (see Cailliet, 1990; Cailliet and Goldman, 2004, for reviews). Estimates of the age at which sexual maturity is attained are influenced by the accuracy of this method, as well as by natural variation among individuals and populations of a species. Gathering accurate and comprehensive reproductive data from pelagic shark populations is critical for enlightened fishery management. Demographic models that utilize life-history parameters are commonly applied to elasmobranchs (Cortés, 2000, 2008; Simpfendorfer, 2004; Au et al., 2008; Smith et al., 2008a). The intrinsic rate of population increase (r), which is a measure of potential growth rate for a population, is commonly estimated by use of life tables or matrix models (age and stage based). Demographic models commonly utilize these reproductive factors: mx, fecundity at age x; α, age at maturity; and w, maximum reproductive age. The net reproductive rate (R0, the average total number of female offspring produced by a single female pup over its lifetime) and mean generation length (G, the mean period between birth of parent and offspring) are calculated from life table data (including number of pups and reproductive rate). R0 is utilized in calculating rm, the innate capacity for increase under particular environmental conditions. Matrix models utilize the finite rate of population increase (λ), which is calculated from reproductive and mortality data (Mollet and Cailliet, 2002). Rebound potential (r2m), or how fast a population will

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increase after fishing pressure has been removed from the population, is a modification of the life table approach that uses, among other parameters, the mean number of pups per litter (b). Because reproductive characteristics may vary between populations, it is very important to characterize these life-history traits throughout the natural geographic range of any species. Our understanding of the reproductive variability of pelagic elasmobranchs is still poor, and much more work is required to improve fisheries models and predictions.

References 1. Aasen, O. (1961) Some Observations on the Biology of the Porbeagle Shark (Lamna nasus L.). ICES C.M. 1961: 109. International Council for the Exploration of the Sea, Copenhagen, Denmark, 7 pp. 2. Aasen, O. (1963) Length and growth of the porbeagle (Lamna nasus, Bonaterre) in the Northwest Atlantic. Fiskerdirektoratets Skrifter, Serie Havundersøkelser 13, 20–37. 3. Amorim, A. F., Arfelli, C. A. and Fagundes, L. (1998) Pelagic elasmobranchs caught by longliners off southern Brazil during 1974–97: An overview. Marine and Freshwater Research 49, 621–632. 4. Au, D. W., Smith, S. E. and Show, C. (2008) Shark productivity and reproductive protection, and a comparison with teleosts. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. 5. Backus, R. H., Springer, S. and Arnold Jr., E. L. (1956) A contribution to the natural history of the white-tip shark, Pterolamiops longimanus (Poey). Deep-Sea Research 3, 178–188. 6. Bane Jr., G. W. (1966) Observations on the silky shark, Carcharhinus falciformis, in the Gulf of Guinea. Copeia 1966, 354–356. 7. Bass, A. J., D’Aubrey, J. D. and Kistnasamy, N. (1973) Sharks of the East Coast of Southern Africa. I. The Genus Carcharhinus (Carcharhinidae). Report No. 33. Oceanographic Research Institute, Durban, South Africa, 168 pp. 8. Bass, A. J., D’Aubrey, J. D. and Kistnasamy, N. (1975) Sharks of the East Coast of Southern Africa. IV. The Families Odontaspididae, Scapanorhynchidae, Isuridae, Cetorhinidae, Alopiidae, Orectolobidae, and Rhiniodontidae. Report No. 39. Oceanographic Research Institute, Durban, South Africa, 102 pp. 9. Bigelow, H. B. and Schroeder, W. C. (1948) Fishes of the Western North Atlantic. Part 1. Lancelets, Cyclostomes, Sharks (eds. A. E. Parr and Y. H. Olsen). Sears Foundation for Marine Research, New Haven, CT, pp. 59–546. 10. Blagoderov, A. I. (1994) Seasonal distribution and some notes on the biology of salmon shark (Lamna ditropis) in the northwestern Pacific Ocean. Journal of Ichthyology 34, 115–121. 11. Bonfil, R. (2008) The biology and ecology of the silky shark, Carcharhinus falciformis. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. 12. Bonfil, R., Mena, R. and de Anda, D. (1993) Biological parameters of commercially exploited silky sharks, Carcharhinus falciformis, from the Campeche Bank, Mexico. In: Conservation Biology of Elasmobranchs (ed. S. Branstetter). NOAA Technical Report NMFS 115. NOAA/ NMFS, Silver Spring, MD, pp. 73–86. 13. Bonfil, R., Clarke, S. and Nakano, H. (2008) The biology and ecology of the oceanic whitetip shark, Carcharhinus longimanus. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK.

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144. Tortonese, E. (1976) A note on Dasyatis violacea (BP) (Plagiostomia, Rajiformes). Bolletino di Pesca Piscicoltura e Idrobiologia 31, 5–8. 145. Uchida, S., Yasuzumi, F., Toda, M. and Okura, N. (1987) On the observations of reproduction in Carcharodon carcharias and Isurus oxyrinchus. Report of the Japanese Group for Elasmobranch Studies 24, 4–6. 146. Uchida, S., Toda, M., Teshima, K. and Yano, K. (1996) Pregnant white sharks and full-term embryos from Japan. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 139–155. 147. Villavicencio-Garayzar, C. J. (1993) Biologia reproductiva de Rhinobatos productus (Pisces: Rhinobatidae), en Bahia Almejas, Baja California Sur, Mexico. Revista de Biologica Tropical 41, 777–782. 148. Wilson, P. C. and Beckett, J. S. (1970) Atlantic Ocean distribution of the pelagic stingray, Dasyatis violacea. Copeia 1970, 696–707. 149. Wintner, S. P. and Cliff, G. (1999) Age and growth determination of the white shark, Carcharodon carcharias, from the east coast of South Africa. Fishery Bulletin 97, 153–169. 150. Yoshimura, H. and Kawasaki, S. (1985) Silky shark (Carcharhinus falciformis) in the tropical water of the western Pacific. Report of the Japanese Group for Elasmobranch Studies 20, 6–10.

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Part II

Life History and Status of Pelagic Elasmobranchs

Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Introduction The current state of knowledge about the biology, ecology, and life histories of 11 of the more abundant species of open ocean elasmobranchs is presented in Chapters 4–13. Although these species inhabit a common environment and face similar threats, they differ in their range, life history, and vulnerability to fisheries, and in the amount of research and conservation attention they have received.

Biology and ecology Elasmobranchs are found in oceanic waters throughout the world, primarily between 70º north and 50º south. Open ocean sharks are apex predators wherever they occur, consuming primarily teleost fish and squid, although shortfin makos (Isurus oxyrinchus; Chapter 7) also eat elasmobranchs off South Africa, and white sharks eat seals and other marine mammals (Carcharodon carcharias; Chapter 5). Colder waters are dominated by porbeagles (Lamna nasus; Chapter 9) in the Southern Hemisphere and the North Atlantic, and by the congeneric salmon shark (L. ditropis; Chapter 8) in the North Pacific. These species, as well as the related white shark and mako sharks, are able to maintain body temperatures above the ambient water temperature, which may explain their broad geographic ranges. Blue sharks (Prionace glauca; Chapter 12), threshers (Alopias spp.; Chapter 4), and pelagic stingrays (Pteroplatytrygon violacea; Chapter 13) are found circumglobally in both temperate and tropical waters. Oceanic whitetips (Carcharhinus longimanus; Chapter 11) and silky sharks (C. falciformis; Chapter 10) are found mainly in the tropical waters of all the world’s oceans. Oceanic whitetips and pelagic threshers (A. pelagicus) are primarily oceanic, whereas the other species are sometimes found near shore. Tagging studies and analyses of data from fisheries have provided information about the movement and population structure of some oceanic sharks. Silky, common thresher (A. vulpinus), shortfin mako, porbeagle, and salmon sharks are known to migrate toward the equator in the winter and to higher latitudes in the summer, presumably to stay within their preferred temperature ranges. Some individuals have been documented to make very long migrations; for example, shortfin mako sharks have traveled 5,500 km in the Pacific (Chapter 7), and white sharks have moved from California to Hawaii (Chapter 6). Migratory patterns related to reproductive behavior can lead to spatial segregation by age and sex, as occurs among blue, oceanic whitetip, and salmon sharks. Although an understanding of population structure and movement is necessary to evaluate the impact of fishing on shark populations, this information is not available for most species. Porbeagles are probably the best studied, and are known to have distinct populations in the Northeast and Northwest Atlantic, which are also probably distinct from the populations in the Southern Hemisphere. Blue and shortfin mako sharks have been extensively tagged in some areas, but the details of their stock structure have not been elaborated. Silky, oceanic whitetip, longfin mako, and thresher sharks are understudied. Pelagic stingrays are the least studied – even the extent of their range has not been well documented. The life histories of the open ocean sharks are quite diverse, although in general the oceanic species tend to be more fecund than the coastal members of their families

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(Chapter 3). Reproductive modes for the pelagic elasmobranchs include aplacental viviparity (thresher, porbeagle, mako, white, and salmon sharks), placental viviparity (blue, oceanic whitetip, and silky sharks), and aplacental viviparity with trophonemata (pelagic stingray); none of the pelagic sharks are oviparous. Females mature at a later age than males for every species examined in Chapter 3, except oceanic whitetips, and generally at a larger size. Mean fecundity ranges from two pups per litter for the bigeye thresher (A. superciliosus) to 26–37 for the blue shark, to more than 60 for shortfin mako, porbeagle, and salmon sharks. These life-history traits constrain the capacity of the pelagic sharks to withstand and rebound from fishing pressure, as discussed in Part 4 of this volume (Chapters 25–27). Chapter 13 includes the first age and growth information published on pelagic stingrays.

Fisheries and status Directed fisheries have been reported for all of the species discussed in this section, except the pelagic stingray. All species including the pelagic stingray are caught as bycatch in fisheries for tuna and other pelagic finfish. Furthermore, fins are taken from all of the oceanic shark species to supply the global fin trade. The carcasses of threshers and shortfin makos are generally retained when they are caught, because their meat is of high value. There is a lack of detailed catch data for sharks, but the available landings and fin trade data suggest that blue sharks are the most commonly caught, followed by silky sharks (Chapter 10). Blue sharks are subject to large catches across the globe; the few available assessments imply that populations are stable in some areas and declining in others (Chapter 12), such as the Northwest Atlantic (Chapter 19). Silky sharks are one of the most common species taken as bycatch in tropical tuna fisheries; they appear to be experiencing growth overfishing off the Atlantic coast of Mexico, but are stable throughout the Pacific (Chapter 10). Some studies have shown declines of oceanic whitetip populations (e.g., in the Gulf of Mexico; Chapter 11), but in general their status is not known. The status of most populations of thresher sharks is also unknown. There is evidence of a decline in an eastern Pacific population of common threshers that was subject to an intensive gill-net fishery in the 1980s. This population has since started to rebuild (Chapter 4). Shortfin makos, which are targeted by both recreational and commercial fisheries, have had stable catch rates in the Pacific, but appear to be declining in the Atlantic (Chapter 7). The status of the salmon shark is not known, but total mortality is probably lower now than it was before high-seas drift-net and salmon fisheries were discontinued (Chapter 8). White sharks are naturally low in abundance, but their current status is unknown and there are no population assessments (Chapter 5). Catch rates have been declining in some areas, which may imply declines in abundance. Fortunately, white sharks are often protected by domestic laws and international agreements, unlike other oceanic sharks. Pelagic stingrays are not targeted by fisheries, but are caught as bycatch in high-seas longline operations (Chapter 13). Nothing is known about their stock structure or population status.

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Conclusion In general, among the pelagic elasmobranchs, commercially important species, temperate species, and species that are found closer to shore (e.g., blue sharks) have received more research attention than the tropical species (e.g., oceanic whitetip). Improved biological information on stock structure and movement, as well as life-history traits, is needed for all species. Most importantly, we are just beginning to compile the species-specific catch and abundance trend data that are necessary to evaluate the status of oceanic sharks. These evaluations are critical if we are to initiate and pursue management measures that will ensure the long-term sustainability of these fisheries.

Chapter 4

The Biology and Ecology of Thresher Sharks (Alopiidae) Susan E. Smith, Randall C. Rasmussen, Darlene A. Ramon and Gregor M. Cailliet

Abstract We review the biology and ecology of the three known species of thresher shark (Alopiidae) occurring in the Atlantic, Pacific, and Indian Oceans: the common thresher shark (Alopias vulpinus), bigeye thresher shark (A. superciliosus), and pelagic thresher shark (A. pelagicus). We also present revised data on age, growth, and sexual maturity of the common thresher shark off California. These new data suggest that off the US West Coast, male and female common threshers mature at ⬃303 cm total length (TL) and ⬃5 years of age. The revised von Bertalanffy growth model for combined data (N
315) produced parameter estimates of L
465 cm TL, K
0.129, and t0
–2.88 (asymptotic length, the von Bertalanffy growth coefficient, and theoretical age at size zero, respectively). Average maximum reproductive age for females is estimated at around 25 years. These results suggest that the common thresher is the fastest-growing and earliest-maturing of the three species of thresher shark, and attains the largest size. Key words: thresher shark, common thresher, bigeye thresher, pelagic thresher, Alopias vulpinus, Alopias superciliosus, Alopias pelagicus, Alopiidae.

Introduction Thresher sharks, or sea foxes, are distinguished by their long, scythelike tails, and make up a small family within the order Lamniformes. They are large, active, and strong-swimming sharks, occurring in oceanic and neritic waters in tropical and temperate seas (Compagno, 1984). They enter the catch of fisheries in various parts of the world and are utilized for their flesh and fins, which are highly regarded for human consumption.

Distribution and movements The common thresher and bigeye thresher are distributed circumglobally in the Atlantic, Pacific, and Indian Oceans and in the Mediterranean, whereas the pelagic thresher is Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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restricted to the Indian and Pacific Oceans (Gruber and Compagno, 1981; Compagno, 1984, 2001). While all occur in the epipelagic zone in both neritic and oceanic waters, there are distributional differences. The best known is the common thresher shark, which is the most frequently encountered in temperate waters and the most coastal of the group, though it also can be found far from land (Compagno, 2001; Smith and Aseltine-Neilson, 2001). It usually occurs within 40–75 miles (72–135 km) of land (Strasburg, 1958; Holts, 1988; Litvinov, 1990) in temperate and occasionally tropical seas over continental and insular shelves and slopes (Compagno, 1984). The pelagic thresher is more oceanic and the most tropical, although distributional information is somewhat hampered by identification problems and confusion with the common thresher. The two are distinguished by a difference in skin color on the sides above the pectoral fin base, which are mottled white in the common thresher and uniformly dusky gray in the pelagic thresher shark. Unlike the pelagic and bigeye, the common thresher has labial folds around the mouth, and the origin of the second dorsal fin is aligned posterior to the free rear tip of the pelvic fin. The bigeye ranges the deepest, making forays into the mesopelagic zone to at least 500 m (Compagno, 1984, 2001). It occurs more commonly in warm temperate to tropical seas, but can nevertheless tolerate cold water temperatures down to 6ºC and can remain at depths in cooler water for longer periods of time than can many other pelagic sharks (H. Nakano, personal communication). It ranges along the continental slope and beyond (Stillwell and Casey, 1976), although inshore catches are also made in neritic waters (Compagno, 1984). The bigeye is easily distinguished from the common and pelagic threshers by its very large, dorsally placed eyes, and unusual sculpted head bearing deep lateral grooves. Movements of these highly active, energetic sharks are largely inferred from seasonal catch patterns and some limited tagging. The common thresher in the Northern Hemisphere apparently undertakes inshore and northerly coastal migrations during the warm season (⬃April to August) in the eastern and western Atlantic and eastern Pacific (Moreno et al., 1989; Bedford, 1992). Recent NMFS satellite pop-up tagging off California documented a southward retreat to warmer waters during winter. Two fish tagged in June 1999 off southern California were re-located off Mexico the following fall and winter, one 270 nautical miles west of Magdelena Bay, Baja California Sur, and the other 510 nautical miles southwest of Cabo San Lucas, Baja California Sur, approximately 172 nautical miles west of Clarión Island, Mexico (Smith and Aseltine-Neilson, 2001). The latter shark, a female of 255 cm total length (TL), was re-located a considerable distance from the mainland when the satellite tag released, but was still less than 40 nautical miles from water less than 200 m deep near Alphecca Bank in the Clarión Fracture Zone. The bigeye is also known to travel long distances, moving 1,000–2,000 miles from the shelf off New Jersey eastward into the central Atlantic and southward into the Gulf of Mexico, and from off North Carolina south to Cuba (Kohler et al., 1998). Short-term tracking of this species in the eastern Pacific revealed pronounced diel vertical movement from deeper (200–550 m) and cooler (6–11ºC) water during the day, upward to the mixed layer (50–130 m) and warmer water temperatures (15–26ºC) at night (H. Nakano, personal communication). Little is known of the movements of the pelagic thresher, except that during El Niño years in the eastern Pacific, a portion of the stock from off Mexico and farther south shifts northward into US West Coast waters (Compagno, 1984; D. B. Holts, personal communication).

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Information is also limited on the stock structure of these widely distributed species, except for genetic work done on the common thresher in the eastern Pacific and some preliminary work on the other species (Eitner, 1995, 1999). Analyses of tissue biopsies from common thresher sharks collected in the Pacific off the US West Coast and Mexico grouped and compared samples from off Oregon/Washington with samples collected off California and Baja California, Mexico; they found no significant differences in haplotypic frequencies, indicating a single homogeneous West Coast population.

Biology and ecology Age and growth The life histories (age, growth, and reproduction) of all three species have been studied to varying degrees. Threshers have intermediate to relatively rapid growth rates compared to other sharks, with growth coefficients ranging from K
0.09 to 0.19; females grow to larger sizes than males (Gruber and Compagno, 1981; Cailliet et al., 1983; Compagno, 1984; Liu et al., 1998, 1999). Cailliet et al. (1983) aged 167 common thresher off the US Pacific Coast and applied published data on size at sexual maturity to their growth curve, concluding that females mature at 260–315 cm TL and 3–4 years, and males at 333 cm TL at 7 years old, under the assumption of one vertebral band pair deposited per year. Here we revise and update this growth curve, using a more precise alternate length to total length conversion and incorporating new data (N
175; 68 males, 107 females) from aged vertebrae collected by California drift-net fishery observers from 1990 to 1999 (Fig. 4.1) and using the same assumption on the periodicity of vertebral banding patterns. We also refine age of maturity, incorporating new gill-net observer data, and eliminate previous unreliable upper-range estimates of female first maturity (e.g., Strasburg’s (1958) Combined growth (Alopias vulpinus)

Total length (cm)

600 500 400

von Bertalanffy parameters Unknown sex Female Male All 83 129 315 n 464.3 464.9 L⬁ 416.2 K 0.189 0.124 0.129 2.879 t0 2.080 3.350

300 200 100 0 0

5

10 15 Number of bands

20

25

Mean sizes/ages at maturity Range Fig. 4.1 Revised Cailliet et al. (1983) von Bertalanffy growth curve for 315 common thresher sharks collected in California/Oregon waters and aged using X-radiography, including 68 male and 107 female new data points. Dashed lines indicate mean ages and sizes of males and females at sexual maturity; the area in gray is the range for males. Von Bertalanffy parameters for males, females, and the total sample are given in the graph insert.

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315-cm-TL specimen was the only pregnant specimen he examined, and Bigelow and Schroeder’s (1948) 427-cm-TL estimate is a speculative one). Taking the mean of the first quartile of 19 drift-net-caught females with fetuses or egg capsules present in the uteri, and noting the rate of increase in size and presence of seminal fluid and calcification in male claspers (N
769), we estimate that females reach maturity at 303 cm TL (160 cm fork length, FL) and 5.3 years old, and males at about the same size and age (4.8 years; 293–311 cm TL, x–
303; 155–165 cm FL, –x
160). Of the three species, the common thresher attains the largest size, reaching a reported maximum of 601 cm TL worldwide and 550 cm TL in the Pacific. The bigeye thresher grows more slowly (K
0.09; Liu et al., 1998), reaches maturity at a much later age, and attains a smaller maximum size of 461 cm TL. Liu et al. (1998), applying Chen et al.’s (1997) reproductive data to their growth curve for bigeye taken off Taiwan, estimated female maturity at 12.3–13.4 years and 332–341 cm TL and male maturity at 9–10 years and 270–288 cm TL. These sizes at maturity agree closely with those in populations examined elsewhere (Stillwell and Casey, 1976; Moreno and Morón, 1992; Chen et al., 1997). The pelagic thresher is the smallest of the three (to about 330 cm TL), reaching its asymptotic length at about the same rate as the bigeye (K
⬃0.09), but maturing earlier. Liu et al. (1999) aged fish from waters off Taiwan and found size at 50% sexual maturity to be 145–150 cm precaudal length (PCL; 282–292 cm TL) and 140–145 cm PCL (267– 276 cm TL) for females and males, respectively. Age at first maturity for females was estimated to be 8.0–9.2 years. Size at birth in the common thresher varies considerably, ranging from 114 to 156 cm TL (Bigelow and Schroeder, 1948; Hixon, 1979; Compagno, 1984; Moreno et al., 1989). Bigeye size at birth is at least 100 cm TL (Moreno and Morón, 1992), averaging between 145 and 149 cm TL (Chen et al., 1997; Liu et al., 1998). Postpartum pelagic threshers range from 158 to 190 cm TL, representing the largest pup-to-maximum-adult size ratio of the three species of Alopias (Liu et al., 1999). Longevity of the common thresher has been widely estimated at 19–50 years (Cailliet et al., 1983; Smith et al., 1998). While the largest female we aged (480 cm TL; 22 years) is smaller than the 550-cm-TL Pacific record, the overall average maximum reproductive age for females may be roughly 25 years off the US West Coast. The bigeye thresher is estimated to live to about 20–21 years (Liu et al., 1998), and the pelagic thresher to 29 years (Liu et al., 1999). Like many other species of sharks, threshers are known to segregate by sex and size. Catches of adults are sexually skewed at certain times and locations off the US West Coast and in the Northeast Atlantic, even though the overall sex ratio in the annual catch may be close to equal (Holts, 1988; Moreno et al., 1989). In the Gulf of Cadiz and waters off northeast Morocco, Moreno et al. (1989) noted sexual segregation of mature adult A. vulpinus, with near-term, female-dominated schools moving shoreward in spring, presumably to give birth to pups in inshore nursery areas. Toward the end of spring, inshore schools are made up of predominantly neonates and pregnant females, to the exclusion of adult males. Sex and size segregation is also noted in the bigeye thresher off the US West Coast, where gill-net catches comprised predominantly large adult males that range north to off Oregon and immature females, which occur mostly south of Monterey Bay and in

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the Southern California Bight. When the pelagic thresher occurs off the US West Coast during El Niño years, females made up 83% of the observed catch.

Reproduction Thresher sharks have an aplacental ovoviviparous reproductive mode. The egg is released from the ovary and then passes down the upper oviduct to the oviducal gland, where presumably fertilization occurs. It is then enclosed in a membranous capsule before passing down into the enlarged lower oviduct or “uterus” to complete development. After fetuses emerge from their membranous shells in early gestation, they are nourished by a supply of yolk-filled egg capsules that continue to be deposited in each oviduct and are consumed in utero as development proceeds (Gubanov, 1978; Gruber and Compagno, 1981; Moreno et al., 1989; Gilmore, 1993). Litter sizes are small. The common thresher usually gives birth to two to four pups (Gubanov, 1978; Cailliet et al., 1983; Bedford, 1992), although broods of up to seven have been recorded off Spain (Moreno et al., 1989), indicating there may be some plasticity in this trait. Litter size of the bigeye is commonly two, rarely four (Moreno and Morón, 1992); that of the pelagic thresher is usually two (Otake and Mizue, 1981; Compagno, 1984; Liu et al., 1999). The common thresher appears to have a seasonal reproductive cycle in various parts of its range; for example, mating presumably takes place in midsummer along the US West Coast and in the northeastern Atlantic (Moreno et al., 1989), with an estimated gestation period of about 9 months (Goldman, 2005). Birth is thought to occur in the spring months in the northeastern Pacific and northeastern Atlantic (Moreno et al., 1989; Bedford, 1992). In Taiwan waters, the reproductive cycle of the bigeye and the pelagic thresher appears not to be seasonal (Chen et al., 1997; Liu et al., 1998, 1999). The gestation period of the bigeye is estimated to be 12 months (Liu et al., 1998); that of the pelagic thresher is unknown, but presumed to be a year or less.

Diet Thresher sharks reportedly feed on small- to medium-sized schooling fishes and pelagic invertebrates such as squid. They have been observed to use their long caudal fin to bunch up, disorient, and stun prey at or near the surface, and are often caught on longlines tailhooked. The common thresher, which feeds on a variety of small schooling species such as anchovy, hake, mackerel, sardine, and squid (Gubanov, 1972; Stick and Hreha, 1989; Bedford, 1992; Preti et al., 2001), is often associated with areas characterized by high biological productivity and the presence of strong frontal zones separating regions of upwelling and adjacent waters, and strong horizontal and vertical mixing of surface and subsurface waters – habitats conducive to production and maintenance of the schooling pelagic prey upon which it feeds (Gubanov, 1978). Bigeye thresher is known to feed on hake, squid, scombrids, alepisaurids, clupeids, istiophorids, and elasmobranchs (Fitch and Craig, 1964; Bass et al., 1975; Stillwell and Casey, 1976; Gruber and Compagno, 1981). Its specialized eyes can roll into upward-directed sockets, possibly allowing it to feed on

Biology and Ecology of Thresher Sharks

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prey silhouetted from above. Results of acoustic telemetry tracking in the eastern Pacific suggest diel vertical migration and primarily night feeding in this species, especially in the area of the thermocline. Tracked individuals have exhibited a nighttime oscillating swimming pattern of slow ascent then rapid descent, perhaps a strategy to maximize upward searching time (H. Nakano, personal communication). The diet of the pelagic thresher is unknown, but presumably it also feeds on small schooling fishes and squid (Compagno, 1984). Like some other pelagic sharks, threshers possess rete systems that may enable them to maintain body heat above that of the surrounding water (Carey et al., 1985; Goldman, 2005), thus allowing them to exploit a broad range of foraging opportunities.

Threats and status The full extent of the worldwide thresher shark harvest is unknown because many fishing nations do not keep detailed landing statistics. Some portion of this harvest may be discarded as bycatch, but because the meat and fins are highly valued (Holts, 1988; Rose, 1996), discards at sea are probably minimal. Where the three species are taken together, the flesh of the common thresher is considered the most palatable and valued (Holts, 1988). Known commercial fishing areas where thresher sharks are targeted or landed incidentally include the US Pacific, Atlantic, and Gulf Coasts; the Caribbean; Uruguay; Northeast Atlantic; Iberian Peninsula and Mediterranean Sea; South Africa; northwest and central Indian Ocean; Taiwan; north central Pacific; western tropical Pacific; New Zealand and southern Australia; Pacific Coast of Mexico and Gulf of California; and Guatemala, Panama, Colombia, and Ecuador (Moreno et al., 1989; Last and Stevens, 1994; Liu et al., 1998; Lasso and Zapata, 1999; Shotton, 1999; Goldman, 2005). Thresher sharks are also sought after by recreational anglers for their fighting ability and food value. The common thresher is moderately productive, and the most productive of the threshers (Cortés, 2008; Smith et al., 2008), but nonetheless has demonstrated its vulnerability under intensive harvest. The population off the US West Coast showed signs of decline less than a decade after a drift-net fishery was developed to target this species in 1977–1978 (Cailliet et al., 1993; Hanan et al., 1993). Since the mid-1980s, area and season restrictions and a shift in much of the fleet’s emphasis to targeting swordfish greatly reduced fishing pressure on this species. This lowered level of fishing effort appears to have allowed a modest amount of stock regrowth, but the population may still be at nearly half of prefishing levels, judging from trends in catch rates (PFMC, 2003). Along the US Pacific Coast, the common, bigeye, and pelagic threshers have recently been included as management unit species in the US Pacific Fisheries Management Council’s Highly Migratory Species Fisheries Management Plan. The plan includes a new regional stock assessment and recommended safe catch guidelines for the common thresher. The status of thresher shark stocks in other parts of the world is less well known. Along the US Atlantic Coast, the common thresher and bigeye thresher are included under the fishery management plan for Atlantic tunas, swordfish, and sharks. A quota has been established for all US Atlantic pelagic sharks, possession of the slow-growing bigeye thresher is prohibited, and a recreational shark bag limit and minimum size have been imposed.

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Acknowledgments We thank Dave Au (NMFS), Ken Goldman (Alaska Department of Fish and Game), Dave Holts (NMFS), and anonymous reviewers for their comments, and Wade Smith and Lynn McMasters for help with the figure. We also gratefully acknowledge the cooperation of drift-net fishery captains and the dedication and work of fishery observers with the National Marine Fisheries Service’s Fishery Observer Branch, Southwest Region, Long Beach, California.

References Bass, A. J., D’Aubrey, J. D. and Kistnasamy, N. (1975) Sharks of the East Coast of Southern Africa. 4. The Families Odontaspididae, Scapanorhynchidae, Isuridae, Cetorhinidae, Alopiidae, Orectolobidae and Rhiniodontidae. Report No. 39. Oceanographic Research Institute, Durban, South Africa, 102 pp. Bedford, D. (1992) Thresher shark. In: California’s Living Marine Resources and Their Utilization (eds. S. Leet, C. M. Dewees and C. W. Haugen). Publication UCSGEP-92-12. California Sea Grant, Davis, CA, pp. 49–51. Bigelow, H. B. and Schroeder, W. C. (1948) Sharks. In: Fishes of the Western North Atlantic. Part 1. Lancelets, Cyclostomes, Sharks (eds. A. E. Parr and Y. H. Olsen). Sears Foundation for Marine Research, New Haven, CT, pp. 59–546. Cailliet, G. M., Martin, L. K., Martin, J. T., Harvey, J. T., Kusher, D. and Welden, B. A. (1983) Preliminary studies on the age and growth of the blue, Prionace glauca, common thresher, Alopias vulpinus, and shortfin mako, Isurus oxyrinchus, sharks from California waters. In: Proceedings of the International Workshop on Age Determination of Oceanic Pelagic Fishes: Tunas, Billfishes, and Sharks (eds. E. D. Prince and L. M. Pulos). NOAA Technical Report NMFS 8. NOAA/NMFS, Silver Spring, MD, pp. 1–17. Cailliet, G. M., Holts, D. B. and Bedford, D. (1993) A review of the commercial fisheries for sharks on the west coast of the United States. In: Shark Conservation (eds. J. Pepperell, J. West and P. Woon). Zoological Parks Board, Mosman, New South Wales, Australia, pp. 13–29. Carey, F. G., Casey, J. G., Pratt Jr., H. L., Urquhart, D. and McCosker, J. E. (1985) Temperature, heat production, and heat exchange in lamnid sharks. Memoirs of the Southern California Academy of Sciences 9, 92–108. Chen, C., Liu, K. and Chang, Y. (1997) Reproductive biology of the bigeye thresher shark, Alopias superciliosus (Lowe, 1839) (Chondrichthyes: Alopiidae), in the northwestern Pacific. Ichthyological Research 44, 227–235. Compagno, L. J. V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 2. Carcharhiniformes. FAO Fisheries Synopsis No. 125. FAO, Rome, Italy, pp. 251–655. Compagno, L. J. V. (2001) FAO Species Catalogue for Fishery Purposes. No. 1. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Vol. 2. Bullhead, Mackerel and Carpet Sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO, Rome, Italy, 269 pp. Cortés, E. (2008) Comparative life history and demography of pelagic sharks. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK.

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Eitner, B. J. (1995) Systematics of the genus Alopias (Lamniformes: Alopiidae) with evidence for the existence of an unrecognized species. Copeia 1995(3), 562–571. Eitner, B. (1999) Contract Progress Report for Proposal No. 97SW01, March 1999. Southwest Fisheries Science Center, NMFS, La Jolla, CA, 4 pp. Fitch, J. E. and Craig, W. L. (1964) First records for the bigeye thresher (Alopias superciliosus) and slender tuna (Allothunnus fallai) from California, with notes on eastern Pacific scombrid otoliths. California Fish and Game Quarterly 50, 195–206. Gilmore, R. G. (1993) Reproductive biology of lamnoid sharks. Environmental Biology of Fishes 38, 95–114. Goldman, K. J. (2005) Thresher shark, Alopias vulpinus. In: Sharks, Rays, and Chimaeras: The Status of the Chondrichthyan Fishes (eds. S. L. Fowler et al.). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 250–252. Gruber, S. H. and Compagno, L. J. V. (1981) Taxonomic status and biology of the bigeye thresher, Alopias superciliosus. Fishery Bulletin 79(4), 617–640. Gubanov, Y. P. (1972) On the biology of the thresher shark [Alopias vulpinus (Bonnaterre)] in the Northwest Indian Ocean. Journal of Ichthyology 12, 591–600. Gubanov, Y. P. (1978) The reproduction of some species of pelagic sharks from the equatorial zone of the Indian Ocean. Journal of Ichthyology 15, 37–43. Hanan, D. A., Holts, D. B. and Coan Jr., A. L. (1993) The California drift gill net fishery for sharks and swordfish, 1981–82 through 1990–91. California Department of Fish and Game Fish Bulletin 175, 95 pp. Hixon, M. A. (1979) Term fetuses from a large common thresher shark, Alopias vulpinus. California Fish and Game Quarterly 65, 191–192. Holts, D. B. (1988) Review of US West Coast commercial shark fisheries. Marine Fisheries Review 50(1), 1–8. Kohler, N. E., Casey, J. G. and Turner, P. A. (1998) NMFS Cooperative Shark Tagging Program, 1962–93: An atlas of shark tag and recapture data. Marine Fisheries Review 60(2), 1–87. Lasso, J. and Zapata, L. (1999) Fisheries and biology of Coryphaena hippurus (Pisces: Coryphaehidae) in the Pacific Coast of Colombia and Panama. In: Biology and Fisheries of Dolphinfish and Related Species (eds. E. Massuti and B. Morales-Nin). Scientia Marina 63 (3–4), 387–399. Last, P. R. and Stevens, J. D. (1994) Sharks and Rays of Australia. CSIRO, Collingwood, Victoria, Australia. Litvinov, F. F. (1990) Structure of epipelagic elasmobranch communities in the Atlantic and Pacific Oceans and their change in recent geologic time. Journal of Ichthyology 29(8), 75–87. Liu, K., Chiang, P. and Chen, C. (1998) Age and growth estimates of the bigeye thresher shark, Alopias superciliosus, in northeastern Taiwan waters. Fishery Bulletin 96, 482–491. Liu, K., Chen, C., Liao, T. and Joung, S. (1999) Age, growth, and reproduction of the pelagic thresher shark Alopias pelagicus in the northwestern Pacific. Copeia 1999(1), 68–74. Moreno, J. A. and Morón, J. (1992) Reproductive biology of the bigeye thresher shark, Alopias superciliosus (Lowe, 1839). Australian Journal of Marine and Freshwater Research 43, 77–86. Moreno, J. A., Parajúa, J. I. and Morón, J. (1989) Biología reproductiva y fenología de Alopias vulpinus (Bonnaterre, 1788) (Squaliformes: Alopiidae) en el Atlántico nor-oriental y Mediterráneo occidental. Scientia Marina 53(1), 37–46. Otake, T. and Mizue, K. (1981) Direct evidence of oophagy in thresher shark, Alopias pelagicus. Japan Journal of Ichthyology 28, 171–172. Pacific Fisheries Management Council (PFMC) (2003) Fishery Management Plan and Environmental Impact Statement for US West Coast Fisheries for Highly Migratory Species. PFMC, Portland, OR.

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Preti, A., Smith, S. E. and Ramon, D. A. (2001) Feeding habits of the common thresher shark (Alopias vulpinus) sampled from the California-based drift gill net fishery, 1998–99. CalCOFI Reports 42, 145–152. Rose, D. A. (1996) An Overview of World Trade in Sharks and Other Cartilaginous Fishes. TRAFFIC International, Cambridge, UK, 106 pp. Shotton, R. (ed.) (1999) Case Studies of the Management of Elasmobranch Fisheries. FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, 479 pp. Smith, S. E. and Aseltine-Neilson, D. (2001) Thresher shark. In: California’s Living Marine Resources: A Status Report (eds. W. S. Leet et al.). Sea Grant Publication SG01-11. California Department of Fish and Game/University of California Agriculture and Natural Resources, Sacramento, CA, pp. 339–341. Smith, S. E., Au, D. W. and Show, C. (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678. Smith, S. E., Au, D. W. and Show, C. (2008) Intrinsic rates of increase in pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Stick, K. C. and Hreha, L. (1989) Summary of the 1988 Washington/Oregon Experimental Thresher Shark Gill Net Fishery. Progress Report 275. Washington Department of Fish and Wildlife, Olympia, WA, 40 pp. Stillwell, C. and Casey, J. G. (1976) Observations on the bigeye thresher, Alopias superciliosus, in the western North Atlantic. Fishery Bulletin 74, 221–225. Strasburg, D. W. (1958) Distribution, abundance, and habits of pelagic sharks in the central Pacific Ocean. Fishery Bulletin 138, 335–361.

Chapter 5

The Biology and Ecology of the White Shark, Carcharodon carcharias Barry D. Bruce

Abstract White sharks (Carcharodon carcharias) occur worldwide, primarily in coastal temperate and subtropical regions, but are occasional visitors to tropical regions. They are known to make open ocean excursions, and some exchange across ocean basins has been documented by tagging and is supported by genetics data. However, global stock structure is still poorly known, and accurate population assessments are not yet possible for any region. Estimates of some biological parameters are available, but most are based on limited data that pool both sexes. White sharks are 120–150 cm total length (TL) at birth. Lengths and estimated ages at maturity are 4.5–5.0 m and 12–17 years for females and 3.6–3.8 m and 7–9 years for males. Females reach larger sizes than males. Maximum length for females is estimated to be at least 6.0 m and longevity estimates range up to 60 years, although the latter is unverified and estimates of 40–50 years may be more reasonable. Estimated growth is 20–30 cm/year in sharks less than 3.0 m, but is poorly documented after maturity. Reported von Bertalanffy growth coefficients (0.058–0.071) are within the range of other lamnids and indicative of slow growth. The gestation period may be up to 18 months with a 3-year reproductive cycle. Reported litter sizes range from 2 to 17 with an embryonic sex ratio of 1:1. White sharks are naturally low in abundance, have low reproductive potential, are believed to have low natural mortality, and presumably have a low capacity for density-dependent compensation to rapid declines in population size. It is therefore reasonable to conclude that populations are vulnerable to recruitment overfishing and all forms of nonnatural mortality. Key words: white shark, Carcharodon carcharias, Lamnidae, fisheries interactions, age and growth.

Introduction White sharks (Carcharodon carcharias, Lamnidae) are large, active, widely occurring, endothermic predators that have attracted considerable notoriety as one of the small number of shark species known to attack humans. Until recently, white sharks were considered Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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largely coastal in distribution and infrequent visitors to oceanic environments. However, their presence at oceanic islands, recent tagging studies, and genetic analyses reveal that individuals may spend considerable periods in the pelagic realm. Although white sharks have been the subject of considerable research over the last two decades, information on several parameters important in assessing the status of world populations is still lacking. This chapter reviews the available biological and fishery information on white sharks.

Distribution, movements, and stock structure Geographic distribution White sharks occur worldwide in temperate and subtropical regions, including all major ocean basins and the Mediterranean Sea (Compagno, 2001). The species has also been recorded at several tropical localities, such as the Coral Sea (Last and Stevens, 1994), Papua New Guinea (Burgess and Callahan, 1996), the central Pacific (Taylor, 1985; Compagno, 2001), northern Brazil (Gadig and Rosa, 1996), and the tropical southwest Indian Ocean (Cliff et al., 2000). White sharks primarily inhabit coastal and offshore waters of continental and insular shelves. They occur from close to the shoreline (including coastal bays and continental islands, and infrequently enter lower reaches of estuaries) to shelf and slope waters. They are recorded throughout continental shelf depths and to at least 1,280 m (Last and Stevens, 1994; Compagno, 2001). There is also a growing body of evidence (including sightings, capture records, and tagging and genetic data) that white sharks make pelagic excursions into ocean basins, although the relative importance of open ocean habitats to the species is unclear. Taylor (1985) confirmed records of white sharks from Hawaiian waters, and the species has been recorded at various other offshore islands, including Noumea and the Marshall and Easter Islands in the Pacific, and the Azores in the Atlantic (Burgess and Callahan, 1996; Fergusson, 1996; Compagno, 2001). Boustany et al. (2002) reported the offshore movements of four out of six white sharks tagged with pop-up archival tags from coastal California into the western Pacific, with one individual moving as far as the Hawaiian Islands (Boustany, 2008). In each case the shark remained entirely pelagic while moving between the surface and depths down to 650–680 m. Bruce and Stevens (2004) reported on two white sharks that moved into oceanic waters off Western Australia, one of which dived to depths of 570 m. Furthermore, a shark tagged off South Australia was reported captured in New Zealand waters (Bruce et al., 2006). Pardini et al. (2001) found genetic evidence suggesting transoceanic movements of male white sharks between South Africa and Australasian waters. Return between South Africa and northwest Australia was documented by Bonfil et al. (2005), also using pop-up archival tags. White sharks are also, though rarely, reported as bycatch in offshore fisheries such as tuna longline and squid fisheries (Compagno, 2001; M. Francis, National Institute of Water and Atmospheric Research, New Zealand, personal communication). Segregation by size and sex has been reported in several areas (Klimley, 1985; Bruce, 1992; Strong et al., 1992; Fergusson, 1996; Ferreira and Ferreira, 1996; Malcolm et al., 2001), although there may be some temporal variability at individual sites (Strong et al., 1996).

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Tagging studies and in situ observations With the exception of the open ocean excursions recorded by Boustany et al. (2002, 2008), Bonfil et al. (2005), and Bruce et al. (2006), tagged sharks have been resighted or recaptured in coastal waters. Coastal distances between tagging and resighting/recapture or those covered during satellite-based tracking have ranged up to 6,000 km and over periods of liberty up to 10 years (Bruce, 1992; Cliff et al., 1996b; Kohler et al., 1998; Malcolm et al., 2001; Bruce et al., 2006). Tracking and observational studies off Australia, South Africa, and both the East and West Coasts of the United States have revealed periods of residency at certain localities interspersed with directed (and sometimes prolonged) periods of traveling, presumably in response to the availability, movements, and behavior of prey species (Ainley et al., 1981; Carey et al., 1982; Klimley, 1985; Anderson and Goldman, 1996; Long et al., 1996; Strong et al., 1996; Malcolm et al., 2001; Boustany et al., 2002; Klimley et al., 2002; Bruce and Stevens, 2004; Bonfil et al., 2005; Bruce et al., 2006). There are also a number of observations of individual white sharks revisiting the same locality after periods of absence ranging from months to years, and in some cases resightings of individuals have occurred repeatedly at the same time of year (Klimley et al., 1992, 2001; Strong et al., 1992, 1996; Anderson and Goldman, 1996; Fergusson, 1996; Ferreira and Ferreira, 1996; Klimley and Anderson, 1996; Goldman and Anderson, 1999; Anderson and Pyle, 2003; Bruce et al., 2005). Klimley and Anderson (1996) concluded that white sharks may be either “transient” or temporary “residents” at pinniped colonies and likened this behavior to the duel social system reported by Baird and Stacey (1988) for killer whales at pinniped colonies off western Canada.

Seasonal movements Captures of white sharks peak during winter and spring off central and northeast Australia (Patterson, 1986; Reid and Krogh, 1992; Malcolm et al., 2001) and off the KwaZuluNatal coast of South Africa (Cliff et al., 1996a), although some captures were recorded year-round. White sharks are seasonally more abundant at the Farallon Islands, California, in autumn (Ainley et al., 1981), and a general pattern of movement north along the California coast in summer followed by return south in autumn/winter was proposed by Klimley (1985). This is supported by the observations of Long et al. (1996), although they also noted that some sharks may live year-round in the waters off central California. Several other studies report the year-round presence of white sharks, although peak sightings may occur over specific periods (Casey and Pratt, 1985; Bruce, 1992; Ferreira and Ferreira, 1996; Malcolm et al., 2001; Bruce et al., 2005).

Effects of temperature White sharks are endotherms (Carey et al., 1982, 1985; Tricas and McCosker, 1984; Goldman et al., 1996), with internal (stomach) temperatures up to 14.3 C° above ambient, and show some evidence of thermoregulation (Goldman, 1997). This may, in part, account for the wide temperature (4.8–26ºC; Casey and Pratt, 1985; Boustany et al., 2002) and geographic range over which the species has been recorded. Correlations of white

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shark activity or seasonality with temperature are generally poor (Bass, 1978; Ferreira and Ferreira, 1996; Pyle et al., 1996), although Pyle et al. (1996) observed an increase in the daily frequency of breaching and surfacing behavior with sea-surface temperature at the Farallon Islands, California. Several studies report either increased captures or periods of heightened activity coinciding with certain water mass characteristics (e.g., Cliff et al., 1996a) and often during periods when various prey species are also present in these areas (Malcolm et al., 2001). These data suggest that white sharks may be responding to the presence or movements of their primary prey species (which may have a temperaturebased cue) rather than to the direct influence of temperature per se.

Stock structure Pardini et al. (2001) provided evidence of philopatry between Australasian and southwest Indian Ocean populations with exchange mediated by males. Direct evidence for longdistance movements by males is scant, although the only white shark caught in Hawaii for which sex was reported by Taylor (1985) was male, and the tagged shark that Boustany et al. (2002) recorded traveling from California to Hawaii was also male. Bonfil et al. (2005), however, recorded the return migration of an immature female white shark between South Africa and Australia, indicating that interpopulation exchange may not be restricted to males. Tagging and genetics data suggest that white sharks in Australia– New Zealand waters form a single population (Pardini et al., 2001; Bruce et al., 2006).

Biology and ecology Age and growth Age and growth in white sharks are poorly documented owing to small sample sizes and the paucity of analyzed vertebrae from large specimens. Reported studies use both precaudal length (PCL) and total length (TL) in growth calculations (see Wintner and Cliff, 1999, for definitions of PCL and TL); conversions are made using the following equations of Cliff et al. (1996a) and Mollet and Cailliet (1996), respectively: TL
1.251 PCL  5.207;

PCL
0.8550 TL  0.0955

Three vertebral-based ageing studies have been published to date from California (Cailliet et al., 1985), South Africa (Wintner and Cliff, 1999), and Australia (Malcolm et al., 2001). Wintner and Cliff (1999) presented the most comprehensive analyses (based on 114 specimens), but their study was restricted to sizes below maturity. The other two studies were based on smaller sample sizes but more comprehensive size ranges (Table 5.1). Insufficient data are available to adequately compare growth between males and females. Annual growth ring deposition (GR, which equals the “bands” of some authors) was assumed by Cailliet et al. (1985) and Malcolm et al. (2001). Wintner and Cliff (1999) found some evidence for annual GR deposition based on a single oxytetracycline-marked shark recaptured after 2.6 years at liberty; however, marginal increment analyses of vertebrae in their

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Table 5.1 Reported Von Bertalanffy growth function parameters for white sharks (sexes combined).* Reference

L (m)

k

t0

n

Size range (m)

Cailliet et al. (1985) Wintner and Cliff (1999) Malcolm et al. (2001)

7.6737 5.44 6.598

0.058 0.065 0.071

3.53 4.4 2.33

21 114 51

1.29–5.079 1.28–3.73 1.4–5.2

Length used TL PCL TL

*L: maximum theoretical length; k: growth constant equal to the rate at which L is reached (Wintner and Cliff, 1999); t0: theoretical number of growth rings at length
zero; n: number of specimens examined in study; TL: total length; PCL: precaudal length.

study were inconclusive. Suitable age validation is thus still lacking for white sharks. All three studies estimated von Bertalanffy growth function (VBF) parameters (Table 5.1), and the results are broadly similar when converted to equivalent length measures. Estimated growth coefficients (k) range from 0.058 to 0.071, indicative of sharks with slow growth (Branstetter, 1990). Various length–weight relationships have been published for white sharks (e.g., Tricas and McCosker, 1984; Casey and Pratt, 1985; Cliff et al., 1996a; Compagno, 2001) and were reviewed by Mollet and Cailliet (1996). Casey and Pratt (1985) noted no significant differences in their length–weight relationships for males and females less than 3.25 m. They also concluded that estimates of weight based on length alone were questionable owing to variability in girth. This variability is particularly apparent over larger sizes (4.0 m) in most studies. Mollet and Cailliet (1996) found that the most accurate equation for predicting weight (mass
M) incorporated both girth (G) and PCL according to the allometric equation: M
46.0 (G2PCL)0.927 Length at birth, based on the maximum sizes reported for embryos and the smallest free-swimming specimens, ranges from approximately 120 to 150 cm TL (Francis, 1996). Estimated growth rates from VBF curves of 20–30 cm/year in sharks less than 3.0 m TL are supported by tag–recapture data (Bruce, 1992; Wintner and Cliff, 1999). Reported sizes at maturity vary widely for both sexes; however, it is clear that males reach maturity at a significantly smaller size than females. The most consistent estimates for onset of maturity are 3.6–3.8 m TL for males (Pratt, 1996; Malcolm et al., 2001) and 4.5–5.0 m TL for females (Francis, 1996), although in both cases the size above which all specimens are mature has not been ascertained. Age estimates (based on published VBF equations) over these size ranges are 7–9 years and 12–17 years for males and females, respectively (Cailliet et al., 1985; Wintner and Cliff, 1999; Malcolm et al., 2001). The maximum lengths of white sharks are clouded in folklore, with reports of “megalodon” specimens variously reported in the literature (see Randall, 1973; Ellis and McCosker, 1991; and references therein). Randall (1973) concluded that the largest reliably measured specimen was 6.0 m TL, and Mollet et al. (1996) considered that the estimates of 7.0 m for two large (but not measured) specimens caught off South Australia and Malta were possible. The latter are similar to L estimates from VBF equations, but the veracity of reports of white sharks over 6.0 m TL is still conjectural.

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The highest reported GR count (23) was reported by Mollet et al. (1996) for a 5.7to 6.00-m-TL white shark from South Africa. Francis (1996) reported 22  1 GR for a 5.36-m-TL individual captured in New Zealand, and Malcolm et al. (2001) reported 21 GR in vertebrae from white sharks of 5.2 and 4.7 m TL. Estimates of longevity based on the time taken to reach 95% of reported VBF L values using the equation 5 ln 2/k (H. Mollet, Moss Landing Marine Laboratories, personal communication) range from 49 to 60 years.

Mortality There have been no direct measures of natural mortality (M ) for the white shark, but it is assumed to be low, based on the low reproductive potential and top-order predator status (Francis, 1997). Cliff et al. (1996b) estimated fishing mortality (F) and total mortality (Z) to be 0.055 and 0.53, respectively, from a limited tagging study (based on 73 tagged sharks and six recaptures). However, they were unable to separate emigration and tag shedding from natural mortality and assumed that M was unlikely to be greater than the 0.18 year1 estimate provided by Aasen (1963) for Lamna nasus. Mollet and Cailliet (2002) estimated M
0.07675 assuming constant mortality and that 1% of the population survives to a maximum age of 60 years. Cortés (2002) estimated mass-specific survival using methods derived by Peterson and Wroblewski (1984), providing estimates of M
0.05–0.14, although he used demographic traits that overestimated fecundity and underestimated life span.

Reproduction Reproduction in white sharks is poorly documented because of the low number of pregnant females that have been reliably examined. Available information has been recently reviewed for females by Francis (1996), and for males by Pratt (1996). The presence of large amounts of yolk in the stomachs of some embryos suggests that white sharks are similar to other lamnid sharks in being aplacental, viviparous, and oophagous (Francis, 1996; Uchida et al., 1996). The captures of pregnant white sharks have been variously reported worldwide, but many are either erroneous or cannot be adequately verified (see Fergusson, 1996; Francis, 1996). Verifiable records (in the form of specimens, photographs, or samples) and detailed accounts have been reported from Japan (Uchida and Toda, 1996; Uchida et al., 1996) and New Zealand (Francis, 1996). There are no data on embryonic developmental rates and the gestation period is unknown, although Francis (1996) suggested that it may be longer than 12 months based on (largely unverified) reports of embryos at various stages of development throughout the year. Mollet et al. (2000) presented evidence that white sharks may have a gestation period of 18 months, and Mollet and Cailliet (2002) have since suggested that this is matched by an 18-month resting period, thus yielding a 3-year reproductive cycle. Some authors have suggested that reproduction in white sharks may be asynchronous (Lineaweaver and Backus, 1970; Francis, 1996), although this has not been confirmed. Reported litter sizes range between 2 and 17 (Norman and Fraser, 1937; Bigelow and Schroeder, 1948; Patterson, 1986; Uchida et al., 1987, 1996; Ellis and McCosker, 1991; Bruce, 1992; Fergusson, 1996; Francis, 1996; Uchida and Toda, 1996; Cliff et al., 2000; Malcolm et al., 2001), with the loss of aborted embryos probably responsible for at least

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some of the lower figures. Francis (1996) suggested that the litter size may range up to 10. The sex ratio of litters, when reported, has generally been close to 1:1. Parturition is believed to occur in spring to summer, based on the capture of neonates and postpartum adults (Klimley, 1985; Fergusson, 1996; Francis, 1996; Uchida et al., 1996), and parturition probably occurs in many, mostly temperate, locations worldwide (Francis, 1996).

Diet The white shark is a versatile predator and feeds on a wide spectrum of prey, including pelagic and demersal finfish (Casey and Pratt, 1985; Bruce, 1992; Fergusson 1996), various other chondrichthyans (Casey and Pratt, 1985), sea turtles (Long, 1996; Fergusson et al., 2000), pinnipeds (Ainley et al., 1981, 1985; Le Boeuf et al., 1982; Tricas and McCosker, 1984; Bruce, 1992; Klimley et al., 1992; Long et al., 1996), cetaceans (Arnold, 1972; Cliff et al., 1989; Long, 1991; Bruce, 1992; Fergusson, 1996), cetacean carrion (Carey et al., 1982; Pratt et al., 1982; Casey and Pratt, 1985; Long et al., 1996), and some invertebrates (e.g., squid and crustaceans; Klimley, 1985; Compagno, 2001). White sharks are also known to kill sea otters off California, although evidence of consuming them has not been found (Ames et al., 1996). White sharks undergo an ontogenetic shift in diet, with marine mammals becoming more important as prey species in specimens over 3–4 m TL (Casey and Pratt, 1985; Klimley, 1985). However, some white sharks in excess of 5 m TL have been found to contain only finfish and chondrichthyans in their stomachs (Malcolm et al., 2001), particularly in areas where the availability of marine mammals is limited. Predatory strategies and attack patterns have been extensively studied around pinniped colonies (see Ainley et al., 1985; McCosker, 1985; Anderson et al., 1996; Klimley et al., 1996; Long et al., 1996; and references therein). Recent observations (based on archival tag data) suggest that some individuals rapidly switch between periods dominated by predation centered around pinniped colonies to very different predatory strategies targeting demersal finfish or chondrichthyans in nearby habitats (Bruce et al., 2006).

Threats and status White sharks are primarily taken as bycatch in several fisheries worldwide, including longline, gill-net, trawl, and handline/rod-and-reel fisheries (Cliff et al., 1996b; Francis, 1996; Uchida et al., 1996; Compagno, 2001; Malcolm et al., 2001), but are also opportunistically fished in a few others (for jaws and other curios; CITES, 2004). White sharks have been entrapped after entering finfish aquaculture cages, ending with either their death (Bruce, 1999) or, in some recent cases, successful release (K. Roda, South Australian Research and Development Institute, personal communication). Catch statistics for most commercial fisheries are poorly recorded, although some attempts have been made to quantify them (e.g., in Australia by Malcolm et al., 2001). White sharks are (or have been) a target species in sports/game fisheries and are sometimes targeted for their nuisance value (for disrupting fishing operations for other species, even in regions where they are currently protected), for retribution for shark attack (Malcolm et al., 2001), or for the high price paid for fins, jaws, and teeth on the international market (Lai, 1983; Chen,

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1996; Rose, 1996). White sharks are also target species in shark control programs in both Australia and South Africa (Reid and Krogh, 1992; Cliff et al., 1996a, b). However, in some cases, these programs now release live sharks (Cliff et al., 1996a; D. Reid, New South Wales Fisheries, personal communication). Estimates of regional population sizes (based on either limited tag–recapture data or a deterministic model assuming sustainable catches) have been made for areas off South Africa and southern Australia (Cliff et al., 1996b; Strong et al., 1996; Malcolm et al., 2001). Declining catch rates of juveniles have been recorded in shark control programs in South Africa and New South Wales (Australia) (Reid and Krogh, 1992; Cliff et al., 1996a), with a decline in mean size reported in the latter study. Catches in a similar program off southern Queensland have not shown strong evidence of decline (G. McPherson, Queensland Department of Primary Industries, personal communication). Significant declines in the ratio of white sharks to other species of sharks taken by gamefishers have been reported in the Mid-Atlantic Bight (Casey and Pratt, 1985) and off eastern Australia (Pepperell, 1992), although these may not take into account changes in targeting behavior by fishers. The white shark has received more international and domestic conservation attention than any other pelagic shark. White sharks are fully protected in the waters of Australia, the United States, South Africa, Malta, and Namibia. New Zealand prohibits targeting of white sharks but allows the sale of those taken as bycatch (CITES, 2004). White sharks are listed as Vulnerable (A1cd; A2cd) on the World Conservation Union (IUCN) Red List (see www.redlist.org/info/categories_criteria1994.html#categories for definitions). In an effort to monitor and stem the trade in white shark parts, Australia and Madagascar jointly nominated the white shark for inclusion on Appendix II of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), and in October 2004 it was listed (see www.fws.gov/international/laws/citestxt.html). This listing requires that all countries monitor and regulate the trade in white sharks (or their parts) to ensure that such trade is not detrimental to the status of white shark populations. White sharks are naturally low in abundance, have low reproductive potential, probably have a low natural mortality, and presumably possess a low capacity for densitydependent compensation to rapid declines in population size. It is therefore reasonable to conclude that populations are vulnerable to recruitment overfishing and all forms of nonnatural mortality (Francis, 1997). However, population status is poorly known over the species range owing to a lack of robust abundance indicators, and quantitative stock assessments are not currently possible.

Acknowledgments Thanks to John Stevens, Henry Mollet, Malcolm Francis, Ian Fergusson, Barbara Block, and Ken Goldman, who provided helpful comments or information for the manuscript.

References Aasen, O. (1963) Length and growth of the porbeagle (Lamna nasus [Bonnaterre]) in the Northwest Atlantic. Fiskerdirektoratets Skrifter, Serie Havundersøkelser 13(6), 20–37.

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Ferreira, C. A. and Ferreira, T. P. (1996) Population dynamics of white sharks in South Africa. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 381–391. Francis, M. P. (1996) Observations on a pregnant white shark with a review of reproductive biology. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 157–172. Francis, M. P. (1997) Reproductive strategy of white sharks, Carcharodon carcharias. Shark News. Newsletter of the IUCN Shark Specialist Group 9, 8–9. Gadig, O. B. F. and Rosa, R. S. (1996) Occurrence of the white shark along the Brazilian coast. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 347–350. Goldman, K. J. (1997) Regulation of body temperature in the white shark, Carcharodon carcharias. Journal of Comparative Physiology and Biology 167, 423–429. Goldman, K. J. and Anderson, S. D. (1999) Space utilization and swimming depth of white sharks, Carcharodon carcharias, at the South Farallon Islands, central California. Environmental Biology of Fishes 56, 351–364. Goldman, K. J., Anderson, S. D., McCosker, J. E. and Klimley, A. P. (1996) Temperature, swimming depth and movements of a white shark at the South Farallon Islands, California. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 111–120. Klimley, A. P. (1985) The areal distribution and autoecology of the white shark, Carcharodon carcharias, off the west coast of North America. Memoirs of the Southern California Academy of Sciences 9, 15–40. Klimley, A. P. and Anderson, S. D. (1996) Residency patterns of white sharks at the South Farallon Islands, California. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 365–373. Klimley, A. P., Anderson, S. D., Pyle, P. and Henderson, R. P. (1992) Spatiotemporal patterns of white shark (Carcharodon carcharias) predation at the South Farallon Islands, California. Copeia 1992, 680–690. Klimley, A. P., Pyle, P. and Anderson, S. D. (1996) The behavior of white sharks and their pinniped prey during predatory attacks. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 175–192. Klimley, A. P., Le Boeuf, B. J., Cantara, K. M., Richert, J. E., Davis, S. F. and Van Sommeran, S. (2001) Radio-acoustic positioning as a tool for studying site-specific behavior of the white shark and other large marine species. Marine Biology 138, 429–446. Klimley, A. P., Beavers, S. C., Curtis, T. H. and Jorgensen, S. J. (2002) Movements and swimming behaviour of three species of sharks in La Jolla Canyon, California. Environmental Biology of Fishes 63, 117–135. Kohler, N. E., Casey, J. G. and Turner, P. A. (1998) NMFS Cooperative Shark Tagging Program, 1962–93: An atlas of shark tag and recapture data. Marine Fisheries Review 60(2), 1–87. Lai, K. E. (1983) Shark fins – processing and marketing in Hong Kong. INFOFISH Marketing Digest 5(83), 35–39. Last, P. R. and Stevens, J. D. (1994) Sharks and Rays of Australia. CSIRO, Collingwood, Victoria, Australia. Le Boeuf, B. J., Riedman, M. and Keyes, R. S. (1982) White shark predation on pinnipeds in California coastal waters. Fishery Bulletin 80, 891–895. Lineaweaver, T. H. and Backus, R. H. (1970) The Natural History of Sharks. Lyons Books, New York.

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Long, D. J. (1991) Apparent predation by a white shark Carcharodon carcharias on a pygmy sperm whale Kogia breviceps. Fishery Bulletin 89, 538–540. Long, D. J. (1996) Records of white shark-bitten leatherback sea turtles along the central Californian coast. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 317–319. Long, D. J., Hanni, K. D., Pyle, P., Roletto, J., Jones, R. E. and Bandar, R. (1996) White shark predation on four pinniped species in central California waters: Geographic and temporal patterns inferred from wounded carcasses. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 263–274. Malcolm, H., Bruce, B. D. and Stevens, J. D. (2001) A Review of the Biology and Status of White Sharks in Australian Waters. CSIRO Marine Research, Hobart, Tasmania, Australia, 81 pp. McCosker, J. E. (1985) White shark attack behaviour: Observations of and speculations about predator and prey strategies. Memoirs of the Southern California Academy of Sciences 9, 123–135. Mollet, H. F. and Cailliet, G. M. (1996) Using allometry to predict body mass from linear measurements of the white shark. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 81–89. Mollet, H. F. and Cailliet, G. M. (2002) Comparative population demography of elasmobranchs using life history tables, Leslie matrices, and stage-based matrix models. Marine and Freshwater Research 53, 503–516. Mollet, H. F., Cailliet, G. M., Klimley, A. P., Ebert, D. A., Testi, A. D. and Compagno, L. J. V. (1996) A review of length validation methods and protocols to measure large white sharks. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 91–108. Mollet, H. F., Cliff, G., Pratt Jr., H. L. and Stevens, J. D. (2000) Reproductive biology of the female shortfin mako Isurus oxyrinchus Rafinesque, 1810, with comments on the embryonic development of lamnoids. Fishery Bulletin 98, 299–318. Norman, J. R. and Fraser, F. C. (1937) Giant Fishers, Whales and Dolphins. Putnam, London, UK. Pardini, A. T., Jones, C. S., Noble, L. R., Kreiser, B., Malcolm, H., Bruce, B. D., Stevens, J. D., Cliff, G., Scholl, M. C., Francis, M., Duffy, C. and Martin, A. P. (2001) Philopatric females and roving male great white sharks. Nature 412, 139–140. Patterson, R. A. (1986) Shark prevention measures working well. Australian Fisheries 45(3), 12–18. Pepperell, J. G. (1992) Trends in the distribution, species composition and size of sharks caught by gamefish anglers off south-eastern Australia, 1961–90. In: Sharks: Biology and Fisheries (ed. J. G. Pepperell). Australian Journal of Marine and Freshwater Research 43(special volume), 213–225. Peterson, I. and Wroblewski, J. S. (1984) Mortality rate of fishes in the pelagic ecosystem. Canadian Journal of Fisheries and Aquatic Sciences 41, 1117–1120. Pratt Jr., H. L. (1996) Reproduction in the male white shark. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 131–138. Pratt Jr., H. L., Casey, J. G. and Conklin, R. E. (1982) Observations on large white sharks, Carcharodon carcharias, off Long Island, New York. Fishery Bulletin 80, 153–156. Pyle, P., Klimley, A. P., Anderson, S. D. and Henderson, R. P. (1996) Environmental factors affecting the occurrence and behavior of white sharks at the Farallon Islands, California. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 281–291. Randall, J. E. (1973) Size of the great white shark (Carcharodon). Science 181, 169–170.

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Reid, D. D. and Krogh, M. (1992) Assessment of catches from protective shark meshing off New South Wales beaches between 1950 and 1990. Australian Journal of Marine and Freshwater Research 43, 283–296. Rose, D. A. (1996) An Overview of World Trade in Sharks and Other Cartilaginous Fishes. TRAFFIC International, Cambridge, UK, 106 pp. Strong, W. R., Murphy, R. C., Bruce, B. D. and Nelson, D. R. (1992) Movements and associated observations of bait-attracted white sharks, Carcharodon carcharias: A preliminary report. In: Sharks: Biology and Fisheries (ed. J. G. Pepperell). Australian Journal of Marine and Freshwater Research 43(special volume), 13–20. Strong Jr., W. R., Bruce, B. D., Nelson, D. R. and Murphy, R. C. (1996) Population dynamics of white sharks in Spencer Gulf, South Australia. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 401–414. Taylor, L. (1985) White sharks in Hawaii: Historical and contemporary records. Memoirs of the Southern California Academy of Sciences 9, 41–48. Tricas, T. C. and McCosker, J. E. (1984) Predatory behaviour of the white shark (Carcharodon carcharias), with notes on its biology. Proceedings of the California Academy of Sciences 43, 221–238. Uchida, S. and Toda, M. (1996) Records of pregnant white sharks from Japanese waters. Kaiyo Monthly 28(6), 371–380. Uchida, S., Yasuzumi, F., Toda, M. and Okura, N. (1987) On the observations of reproduction in Carcharodon carcharias and Isurus oxyrinchus. Report of the Japan Group for Elasmobranch Studies 24, 4–6. Uchida, S., Toda, M., Teshima, K. and Yano, K. (1996) Pregnant sharks and full-term embryos from Japan. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 139–155. Wintner, S. P. and Cliff, G. (1999) Age and growth determinations of the white shark Carcharodon carcharias, from the east coast of South Africa. Fishery Bulletin 97, 153–169.

Chapter 6

Case Study: White Shark Movements in the North Pacific Pelagic Ecosystem Andre M. Boustany, Kevin C. M. Weng, Scot D. Anderson, Peter Pyle and Barbara A. Block

Abstract The advent of novel electronic tracking technologies has allowed researchers to study the movements of ocean animals in their natural environment. Pop-up tagging of adult white sharks off the coast of central California provided insight into the movement patterns and environmental preferences of these sharks in the North Pacific Ocean. Tagged white sharks spent long periods, up to 8 months, in the pelagic ecosystem and far from land. While offshore, sharks experienced a wide range of depths and temperatures. The purpose of these offshore excursions remains unknown, but further tagging over wider size ranges and geographic areas should help to address these questions. Key words: white shark, Carcharodon carcharias, satellite tagging, Lamnidae, pelagic shark movement, North Pacific.

Introduction White sharks (Carcharodon carcharias, Lamnidae) are large apex predators with the capability to conserve metabolic heat and maintain body temperatures warmer than ambient (Carey et al., 1971, 1982; Goldman et al., 1996; Goldman, 1997). They are found in all major ocean basins, from temperate to tropical seas, although most visual identifications have been from temperate waters (Compagno, 2001). Traditionally, white sharks were considered primarily coastal in nature, aggregating around pinniped colonies to feed (Klimley, 1985; Long et al., 1996). Yet occasional sightings of white sharks far from land (Compagno, 2001), their occurrence at oceanic islands (Taylor, 1985), and genetic studies suggesting movement between continents (Pardini et al., 2001) indicate that they are capable of making long-distance, open ocean migrations. However, it has been difficult to study white sharks within and across the entire pelagic ecosystem. Recent advances in satellite telemetry have overcome this limitation by allowing researchers to track pelagic fishes far from land, independent of research vessels (Block et al., 1998). Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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One of the newest electronic tagging technologies is the pop-up satellite archival tag (PSAT; Block et al., 1998; Marcinek et al., 2001). These tags are attached externally to marine animals, where they collect pressure, ambient temperature, and light-level data at user-defined intervals. At a preprogrammed date, the tags release from the fish, float to the surface, and transmit summaries of stored data to researchers through the Argos satellite system. Light-level data in conjunction with tag-recorded sea surface temperatures (SST) can be used to estimate longitude and latitude (Wilson et al., 1992; Teo et al., 2004).

Methods and Results Between 1999 and 2003, 25 adult (3.7–5.3 m) white sharks were tagged with PSATs at Southeast Farallon Island (SEFI), off the central coast of California (Boustany et al., 2002). White sharks are present at SEFI in the fall and early winter but are absent at other times of the year (Ainley et al., 1985). Males return to the island yearly, but females are believed to return on alternate years (Anderson and Pyle, 2003), suggesting a biennial breeding period. It is currently unknown where breeding or pupping takes place in the North Pacific. To examine the horizontal and vertical movement patterns of white sharks when not at SEFI, PSATs were applied to the dorsal musculature of the sharks for periods ranging from 14 to 274 days. To date, 12 tags have successfully reported data through the satellites. Tagged sharks remained in the vicinity of SEFI for periods ranging from 0.5 to 4 months after tagging. Previous acoustic studies have indicated that white sharks are actively searching for prey at this time (Goldman et al., 1996; Goldman and Anderson, 1999; Klimley et al., 2001). While in this area, temperature ranges were narrow (8–14ºC) and diving was shallow as sharks were restricted by the continental shelf. Sharks spent the majority of time (⬎95%) between the surface and 50 m depth. In the late fall and early winter, sharks moved offshore toward the southwest, taking them into the warmer temperatures of the eastern Pacific’s subtropical gyre (Fig. 6.1). The earliest movements off the continental shelf took place in late November, whereas other sharks remained near the tagging location until early March. As the white sharks moved offshore, diving increased with maximum dive depths extending below 700 m. Deeper diving, coupled with movement into subtropical waters, expanded the temperature range that sharks experienced (4.6–26.2ºC). One male shark showed movement to the Hawaiian Islands in 2 consecutive years, remaining in the area for at least 4 months before returning to SEFI (Boustany et al., 2002). Reports of white shark predation on cetaceans near the Hawaiian Islands and the timing of the shark’s arrival with the humpback whale calving season suggest that movement to that area may be for feeding (J. Naughton, National Marine Fisheries Service, personal communication). All other white sharks that were tracked for longer than 1 month moved toward a region of the subtropical eastern Pacific midway between Baja California and the Hawaiian Islands (Fig. 6.1). This region is characterized by a lack of seamounts, strong temperature gradients, or prominent currents, raising the question of why white sharks are attracted to this area. These sharks remained in this area for up to 8 months with no observed movement back to California coastal areas, suggesting that the period of

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160ºW

150ºW

140ºW

130ºW

120ºW

110ºW

40ºN

䉱

30ºN

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Fig. 6.1 Release location (black triangle) and pop-up locations of male (white circles) and female (gray circles) white sharks tagged between 1999 and 2003.

pelagic residency may be a significant portion of their yearly cycle. Depths recorded by the tags indicate that sharks were routinely making deep dives (⬎300 m) while in this region. The fact that subadult white sharks tracked off the coasts of California, Australia, and South Africa have not shown extensive periods of pelagic residency (K. C. M. Weng et al., unpublished data; Bonfil et al., 2005; Bruce, 2008) suggests that these movements may be related to breeding in adult sharks. Although young-of-the-year white sharks are found predominantly in southern California waters (Klimley, 1985; Dewar et al., 2004), it remains possible that these small sharks may have traveled to coastal areas from elsewhere. However, the possibility of an offshore pupping ground does not explain the movement of males into pelagic waters. Because current hypotheses regarding duration of gestation suggest an 18-month time period, it seems unlikely that mating and pupping would occur over the same period (Mollet et al., 2000), and it is thus possible that sharks travel to this offshore area to mate (Anderson and Pyle, 2003). Electronic tags have revealed new insights into the pelagic behaviors of white sharks. It remains uncertain whether white sharks of differing size classes and from other geographic areas exhibit similar movement patterns as these adult white sharks tracked in the eastern North Pacific. Ongoing tagging of both adolescent sharks in the eastern Pacific as well as adult sharks off Australia and South Africa should help to discern the influences of tagging location and ontogenetic shifts in behavior on the pelagic residency of white sharks. Such data will improve our understanding of white shark movements and will be critical to establishing protective measures to conserve these populations worldwide.

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References Ainley, D. G., Henderson, R. P., Huber, H. R., Boekelheide, R. J., Allen, S. G. and McElroy, T. L. (1985) Dynamics of white shark/pinniped interactions in the Gulf of the Farallones. Memoirs of the Southern California Academy of Sciences 9, 109–122. Anderson, S. D. and Pyle, P. (2003) A temporal, sex specific occurrence pattern among white sharks at the South Farallon Islands, California. California Fish and Game 89(2), 96–101. Block, B. A., Dewar, H., Farwell, C. and Prince, E. D. (1998) A new satellite technology for tracking the movements of Atlantic bluefin tuna. Proceedings of the National Academy of Sciences 95(16), 9384–9389. Bonfil, R., Meyer, M., Scholl, M. C., Johnson, R., O’Brien, S., Oosthuizen, H., Swanson, S., Kotze, D. and Paterson, M. (2005) Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science 310, 100–103. Boustany, A. M., Davis, S. F., Pyle, P., Anderson, S. D., Le Boeuf, B. J. and Block, B. A. (2002) Expanded niche for white sharks. Nature 415, 35–36. Bruce, B. D. (2008) The biology and ecology of the white shark, Carcharodon carcharias. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Carey, F. G., Teal, J. M., Kanwisher, J. W., Lawson, K. D. and Beckett, J. S. (1971) Warm bodied fish. American Zoologist 11, 137–145. Carey, F. G., Kanwisher, J. W., Brazier, O., Gabrielson, G., Casey, J. G. and Pratt, H. L. (1982) Temperature and activities of a white shark, Carcharodon carcharias. Copeia 1982(2), 254–260. Compagno, L. J. V. (2001) FAO Species Catalogue for Fishery Purposes. No. 1. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Vol. 2. Bullhead, Mackerel and Carpet Sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO, Rome, Italy, 269 pp. Dewar, H., Domeier, M. and Nasby-Lucas, N. (2004) Insights into young of the year white shark, Carcharodon carcharias, behavior in the Southern California Bight. Environmental Biology of Fishes 70, 133–143. Goldman, K. J. (1997). Regulation of body temperature in the white shark, Carcharodon carcharias. Journal of Comparative Physiology and Biology 167, 423–429. Goldman, K. J. and Anderson, S. D. (1999). Space utilization and swimming depth of white sharks, Carcharodon carcharias, at the South Farallon Islands, central California. Environmental Biology of Fishes 56, 351–364. Goldman, K. J., Anderson, S. D., McCosker, J. E. and Klimley, A. P. (1996) Temperature, swimming depth, and movements of a white shark at the South Farallon Islands, California. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 111–120. Klimley, A. P. (1985) The areal distribution and autoecology of the white shark, Carcharodon carcharias, off the West Coast of North America. Memoirs of the Southern California Academy of Sciences 9, 15–40. Klimley, A. P., Le Boeuf, B. J., Cantara, K. M., Richert, J. E., Davis, S. F., Van Sommeran, S. and Kelly, J. T. (2001) The hunting strategy of white sharks (Carcharodon carcharias) near a seal colony. Marine Biology 138, 617–636. Long, D. J., Hanni, K. D., Pyle, P., Roletto, J., Jones, R. E. and Bandar, R. (1996) White shark predation on four pinniped species in central California waters: Geographic and temporal patterns inferred from wounded carcasses. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 263–274.

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Marcinek, D. J., et al. (2001) Depth and muscle temperature of Pacific bluefin tuna examined with acoustic and pop-up satellite tags. Marine Biology 138, 869–885. Mollet, H. F., Cliff, G., Pratt Jr., H. L. and Stevens, J. D. (2000) Reproductive biology of the female shortfin mako Isurus oxyrinchus Rafinesque, 1810, with comments on the embryonic development of lamnoids. Fishery Bulletin 98, 299–318. Pardini, A. T., Jones, C. S., Noble, L. R., et al. (2001) Sex-biased dispersal of great white sharks. Nature 412, 139–140. Taylor, L. (1985) White sharks in Hawaii: Historical and contemporary records. Memoirs of the Southern California Academy of Sciences 9, 41–48. Teo, L. H. T., Boustany, A. M., Blackwell, S., Walli, A., Weng, K. C. and Block, B. A. (2004) Validation of geolocation estimates based on light level and sea surface temperature from electronic tags. Marine Ecology Progress Series 283, 81–98. Wilson, R. P., Ducamp, J. J., Rees, G. W., Culik, B. M. and Niekamp, K. (1992) Estimation of location: Global coverage using light intensity. In: Wildlife Telemetry: Remote Monitoring and Tracking of Animals (eds. I. G. Priede and S. M. Swift). Ellis Horwood, London, UK, pp. 131–134.

Chapter 7

The Biology and Ecology of the Shortfin Mako Shark, Isurus oxyrinchus John D. Stevens

Abstract The shortfin mako (Isurus oxyrinchus) is a pelagic oceanic species with a widespread distribution in temperate and tropical waters of all the world’s oceans. It is a target species in some areas, but is principally caught as bycatch of longline and gill-net fisheries directed at tuna and billfish. It is also an important recreational species in many regions. Reproduction is by aplacental viviparity with embryonic oophagy, and the average litter size is 12; captures of pregnant females are relatively uncommon. Breeding frequency appears to be every 3 years, giving an annual fecundity of four. There is a large sexual difference in the size at maturity, with males maturing at about 195 cm total length, while females do not mature until 265–280 cm. Published information on growth rates and age estimates are conflicting, and further studies are required to resolve age and growth in this species. Little is known about stock structure or population status, although most populations do not (yet) appear to have been severely impacted by fishing pressure. Key words: shortfin mako, Isurus oxyrinchus, Lamnidae, fisheries, population status.

Introduction The shortfin mako (Isurus oxyrinchus, Lamnidae) is among the most active and powerful of fishes and, like other members of the lamnid family, it is endothermic, paralleling the adaptations of the scombrid tunas. This species is a popular sport fish and is a common bycatch of pelagic longline fisheries, where it is retained for both meat and fins. Despite its common capture, the biology of the shortfin mako is not well known, with conflicting information on growth rates (Cailliet et al., 1983; Pratt and Casey, 1983) and relatively few captures of pregnant females leading to gaps in our knowledge of the reproductive cycle and annual fecundity (Mollet et al., 2000). As with other shark species commonly taken by longline fisheries, there is concern over its population status, with recent literature suggesting significant declines in certain areas (Baum and Myers, 2004). The generally poor quality of the data associated with bycatch species results in catch-rate standardization problems, and makes it difficult to determine the effects of fishing on this species (and other pelagic sharks). Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Biology and ecology Age and growth Currently, there is considerable uncertainty associated with age and growth of the shortfin mako, relating to whether one or two growth bands are produced each year (Cailliet et al., 1983; Pratt and Casey, 1983). Pratt and Casey (1983) believed that two bands were formed each year in the Northeast Atlantic, resulting in a relatively fast growth rate with maturity reached at about 2.5 years for males (195 cm total length, TL) and 6 years for females (265–280 cm TL; Table 7.1). Cailliet et al. (1983) aged a small sample of shortfin makos from the Pacific and, because they considered that one growth band was formed annually, reported a growth rate about half as fast as that from the Atlantic. Formation of one band each year now seems most likely (Ardizzone et al., 2006; Bishop et al., 2006; Natanson et al., 2006), but stronger evidence of this must await further study. The oldest aged fish was 17, with longevity estimated to be 45 years; maximum size is about 4 m.

Table 7.1 Shortfin mako life-history parameters (all lengths are cm TL). Length at birth

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Length at first maturity

M: 195 F: 265–280

Stevens (1983) Cliff et al. (1990)

Length at median maturitya

M: 197–202 F: 301–312

Francis and Duffy (2005)

Maximum length

M: 296 F: 396

Compagno (2001)

Age at first maturityb (years)

M: 2.5; F: 5 M: 9

Pratt and Casey (1983) Cailliet et al. (1983)

Age at median maturity (years)

M: 7 F: 19

Bishop et al. (2006)

Age at recruitment (year)

0–1

Stevens and Wayte (1999)

Longevity (years)

11.5–17 (oldest aged) 45 (estimated longevity)

Pratt and Casey (1983) Cailliet et al. (1983)

Growth

M: TL = 302 (1
e
0.266(t1.0)) F: TL = 345 (1
e
0.203(t1.0)) M  F: TL = 321 (1
e
0.072(t3.75))

Pratt and Casey (1983) Cailliet et al. (1983) Mollet et al. (2000)

Reproduction

Aplacental viviparity

Litter size (number)

Average 12, maximum 25

Mollet et al. (2000, 2002)

Litter size increases with maternal size

LS  0.810 TL2.346 n = 24; r2  0.25

Mollet et al. (2000)

Gestation (months)

15–18

Mollet et al. (2000)

Breeding frequency (years)

3

Mollet et al. (2000)

Annual fecundity (number)

Average 4

Mollet et al. (2000)

Pupping season

Mainly late winter to spring

Mollet et al. (2000)

Sex ratio of embryos (M:F)

Approximately 1:1 (57:68 based on 10 liters)

Mollet et al. (2000)

a

Length at which 50% of the individuals are mature. Using the lengths at first maturity in this table.

b

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Reproduction The reproductive method in the shortfin mako is aplacental viviparity with embryonic oophagy (Snelson et al., 2008), but there are relatively few records of pregnant females. Litters of 4–25 pups (average 12), which are about 70 cm TL at birth, are born after a gestation period of 15–18 months (Mollet et al., 2000, 2002). Litter size increases with maternal size (Mollet et al., 2000). The reproductive cycle appears to be 3 years. Parturition generally occurs from late winter to spring in both hemispheres, but may extend into summer (Duffy and Francis, 2001). On the basis of the majority of reports, nursery areas appear to be situated close to the coast.

Diet The diet of shortfin makos studied in the Northwest Atlantic and off Australia consisted mainly of teleost fish and cephalopods (Stillwell and Kohler, 1982; Stevens, 1984), while elasmobranchs were the most common prey category from Natal, South Africa (Cliff et al., 1990). A daily ration of 2 kg/day (based on an average weight of 63 kg) was estimated for shortfin makos in the Northwest Atlantic (Stillwell and Kohler, 1982). Large shortfin makos over 3 m in length have very broad, more flattened and triangular teeth, perhaps better suited to cutting large prey than the awl-shaped teeth of smaller individuals (Compagno, 2001). There are several anecdotal accounts of shortfin makos attacking and consuming broadbill swordfish (Xiphias gladius).

Distribution and movements Distribution The shortfin mako is found throughout temperate and tropical waters of all oceans from about 50ºN (up to 60ºN in the Northeast Atlantic) to 50ºS (Compagno, 2001). It occurs from the surface to at least 600 m depth; although primarily oceanic, it is occasionally found close inshore where the continental shelf is narrow. It is not often found in waters below 13ºC, though catches have been made in 10ºC surface temperatures in the South Pacific (Yatsu, 1995). Satellite telemetry has documented vertical excursions to 600 m depth (J. D. Stevens, unpublished data). Of two largish individuals acoustically tracked in the Atlantic, one moved between the surface and 450 m, while the other dived to over 400 m but rarely came up above 100 m, possibly avoiding the upper mixed layer (Carey et al., 1981; Carey and Scharold, 1990). Tracking studies of 1.7- to 1.8-m-TL juveniles in the California Bight showed that they spent 90% of their time in the mixed layer (15 m), with only infrequent excursions below the thermocline (Holts and Bedford, 1993).

Migration and movements Results from a large tagging study in the Northwest Atlantic showed that shortfin makos make extensive movements of up to 4,542 km, with 36% of recaptures caught at greater than 556 km from their tagging site (Casey and Kohler, 1992). However, only one fish

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crossed the Mid-Atlantic Ridge, suggesting that trans-Atlantic migrations are not as common as in blue sharks (Prionace glauca). Casey and Kohler (1992) proposed the following hypothesis for shortfin mako migrations in the western North Atlantic. During winter they are found along the western margin of the Gulf Stream north to Cape Hatteras; from January to April they are seldom taken on the continental shelf north of Cape Hatteras. In April and May, as inshore shelf waters start to warm and the axis of the Gulf Stream moves farther north, shortfin makos start to move onto the shelf between Cape Hatteras and Georges Bank. From June to October they are present on the shelf between Cape Hatteras and the southern Gulf of Maine, as well as offshore to the Gulf Stream. These authors suggest that this area may be the primary feeding grounds for a large part of the juvenile and subadult population in the western North Atlantic. During autumn and winter, shortfin makos move offshore and south to wintering grounds in the Gulf Stream and Sargasso Sea, with some also entering the Caribbean and Gulf of Mexico. The core distribution in the western North Atlantic seems to be between 20ºN and 40ºN and bordered by the Gulf Stream in the west and the Mid-Atlantic Ridge in the east (Casey and Kohler, 1992). More limited data from the Pacific also show large movements of up to 5,500 km, although most tag returns from New Zealand and southeast Australia are restricted to the southwest Pacific (Davies and Hartill, 1998; Hartill, 1999; Hartill and Davies, 1999; Holdsworth and Saul, 2003; K. Thompson, FRI, Sydney, Australia, personal communication; J. D. Stevens, unpublished data). The shortfin mako is probably the fastest shark and is among the most active and powerful of fishes; it is renowned for its jumps well clear of the water when hooked on sportfishing gear. This species, like other lamnid sharks, is endothermic in using a heatexchanging circulatory system to maintain muscle and visceral temperatures above that of the surrounding seawater, thereby allowing a higher level of activity (Carey et al., 1981).

Threats and status Fisheries Some small target fisheries for shortfin mako exist, for example, in California and Spain, but the majority of the catch is taken incidentally by longlines and gill nets directed at tuna and billfish (Holts et al., 1998). Consequently the magnitude of the catch and mortality is not reflected in catch statistics. Stevens (2000) estimated that 12,500 metric tons (t; erroneously printed as 4,100 t) of shortfin makos were caught by longline fleets in the Pacific in 1994, and Babcock and Nakano (2008) reported that about 10,000 t were caught by tuna fleets in the Atlantic in 1995. Other annual catches from smaller areas or more specific fisheries are generally between 20 and 800 t (Mejuto, 1985; Muñoz-Chápuli et al., 1993; Bonfil, 1994; Stevens and Wayte, 1999; Francis et al., 2001). In general, shortfin mako catches tend to be about 3–13% of blue shark catches in the same longline or gill-net fishery. For anglers, the shortfin mako is the most desirable and commonly retained big game shark because it puts up a good fight and has high-quality meat (Babcock, 2008). Casey and Hoey (1985) stated that the recreational catch of shortfin makos along the US Atlantic Coast and in the Gulf of Mexico in 1978 was 17,973 fish weighing some 1,223 t, but only

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2,882 makos were reported in 2001 (Babcock, 2008). Between 1987 and 1989, this catch was about 1,000 t/year (Casey and Kohler, 1992). High-seas longline fisheries generally catch shortfin makos between 65 and 375 cm TL, with most being between 110 and 270 cm TL (Buencuerpo et al., 1998; Stevens and Wayte, 1999; Francis et al., 2001). Francis et al. (2001) estimated that 20–59% of males and 1–4% of females were mature in New Zealand longline catches, depending on region. Some fisheries, particularly in coastal areas, catch much smaller fish. Holts et al. (1998) reported average lengths of 130 cm TL in the California drift-net fishery. In Australia, 82% of gamefish-caught shortfin makos were less than 100 kg (Pepperell, 1992).

Stock structure and status Heist et al. (1996) and Heist (2008) used mitochondrial DNA to examine genetic population structure based on samples from the North and South Atlantic and Pacific Oceans. Their data did not support the presence of genetically distinct stocks, although the North Atlantic population appeared to be isolated from that of the South Atlantic. The lack of significant differences in haplotype frequencies between the North and South Pacific and South Atlantic does not necessarily mean there is only one panmictic stock in these widely separated areas, as only a very small number of migrants are necessary to homogenize the stock. Population assessments for shortfin mako are limited. There are few data that reflect long-term catch per unit effort (CPUE) trends for this species. Nakano and Honma (1996) presented CPUE data for the tuna longline fishery in the Atlantic over the period 1971–1994 that were considered to reflect mainly shortfin mako. The data did not show a marked trend over this period either north of 20ºN, from 20ºN to 20ºS, or south of 20ºS. Babcock and Nakano (2008), reporting on the International Commission for the Conservation of Atlantic Tunas (ICCAT) bycatch working group’s population assessment of shortfin mako, note that populations have declined in both the North and South Atlantic. Populations may be below the biomass that would sustain maximum sustainable yield in the North Atlantic, as CPUE trends suggest depletions of 50% or more. Baum et al. (2003) estimated that all large coastal and oceanic sharks caught by pelagic longline in the Northwest Atlantic had declined by more than 50% in the past 8–15 years, with the exception of makos (both species combined), which showed “moderate declines.” However, in the Gulf of Mexico, Baum and Myers (2004) showed that standardized catch rates of mako sharks (both species combined) declined from 0.19 in the 1950s to 0.09 in the 1990s. The assessment of the population status of shortfin makos and other pelagic sharks is hampered by the generally poor data quality associated with bycatch species in long-line fisheries, and by problems with CPUE standardization. Hence it is difficult to determine the degree of fishing pressure experienced by these species, and whether current fishing rates are sustainable.

References Ardizzone, D., Cailliet, G. M., Natanson, L. J., Andrews, A. H., Kerr, L. A. and Brown, T. A. (2006) Application of bomb radiocarbon chronologies to shortfin mako (Isurus oxyrinchus) age validation. Environmental Biology of Fishes 77, 355–366.

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Babcock, E. A. (2008) Recreational fishing for pelagic sharks worldwide. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Babcock, E. A. and Nakano, H. (2008) Data collection, research, and assessment efforts for pelagic sharks by the International Commission for the Conservation of Atlantic Tunas. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Baum, J. K. and Myers, R. A. (2004) Shifting baselines and the decline of pelagic sharks in the Gulf of Mexico. Ecology Letters 7, 135–145. Baum, J. K., Myers, R. A., Kehler, D. G., Worm, B., Harley, S. J. and Doherty, P. A. (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299(5605), 389–392. Bishop, S. D. H., Francis, M. P., Duffy, C. and Montgomery, J. C. (2006) Age, growth, maturity, longevity and natural mortality of the shortfin mako shark (Isurus oxyrinchus) in New Zealand waters. Marine and Freshwater Research 57, 143–154. Bonfil, R. (1994) Overview of World Elasmobranch Fisheries. FAO Fisheries Technical Paper No. 341. FAO, Rome, Italy, 119 pp. Buencuerpo, V., Ríos, S. and Morón, J. (1998) Pelagic sharks associated with the swordfish, Xiphias gladius, fishery in the eastern North Atlantic Ocean and the Strait of Gibraltar. Fishery Bulletin 96, 667–685. Cailliet, G. M., Martin, L. K., Harvey, J. T., Kusher, D. and Welden, B. A. (1983) Preliminary studies on the age and growth of blue, Prionace glauca, common thresher, Alopias vulpinus, and shortfin mako, Isurus oxyrinchus, sharks from California waters. In: Proceedings of the International Workshop on Age Determination of Oceanic Pelagic Fishes: Tunas, Billfishes, and Sharks (eds. E. D. Prince and L. M. Pulos). NOAA Technical Report NMFS 8. NOAA/NMFS, Silver Spring, MD, pp. 179–199. Carey, F. G. and Scharold, J. V. (1990) Movements of blue sharks (Prionace glauca) in depth and course. Marine Biology 106, 329–342. Carey, F. G., Teal, J. M. and Kanwisher, J. W. (1981) The visceral temperature of mackerel sharks (Lamnidae). Physiological Zoology 54, 334–344. Casey, J. G. and Hoey, J. J. (1985) Estimated catches of large sharks by US recreational fishermen in the Atlantic and Gulf of Mexico. In: Shark Catches from Selected Fisheries off the US East Coast. NOAA Technical Report NMFS SSRF No. 31. NOAA/NMFS, Silver Spring, MD, pp. 15–19. Casey, J. G. and Kohler, N. E. (1992) Tagging studies on the shortfin mako (Isurus oxyrinchus) in the western North Atlantic. In: Sharks: Biology and Fisheries (ed. J. G. Pepperell). Australian Journal of Marine and Freshwater Research 43(special volume), 45–60. Cliff, G., Dudley, S. F. J. and Davis, B. (1990) Sharks caught in the protective gill nets of Natal, South Africa. 3. The shortfin mako shark Isurus oxyrinchus (Rafinesque). South African Journal of Marine Science 9, 115–126. Compagno, L. J. V. (2001) FAO Species Catalogue for Fishery Purposes. No. 1. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Vol. 2. Bullhead, Mackerel and Carpet Sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO, Rome, Italy, 269 pp. Davies, N. M. and Hartill, B. (1998) New Zealand Billfish and Gamefish Tagging 1996–97. NIWA Technical Report 35. National Institute of Water and Atmospheric Research, Wellington, New Zealand, 12 pp. Duffy, C. and Francis, M. P. (2001) Evidence of summer parturition in shortfin mako (Isurus oxyrinchus) sharks from New Zealand waters. New Zealand Journal of Marine and Freshwater Research 35, 319–324.

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Francis, M. P. and Duffy, C. (2005) Length at maturity in three pelagic sharks (Lamna nasus, Isurus oxyrinchus and Prionace glauca) from New Zealand. Fishery Bulletin 103, 489–500. Francis, M. P., Griggs, L. H. and Baird, S. J. (2001) Pelagic shark bycatch in the New Zealand tuna longline fishery. Marine and Freshwater Research 52, 165–178. Hartill, B. (1999) Billfish and gamefish tagging. Seafood New Zealand, May, 26–27. Hartill, B. and Davies, N. M. (1999) New Zealand Billfish and Gamefish Tagging 1997–98. NIWA Technical Report 57. National Institute of Water and Atmospheric Research, Wellington, New Zealand, 15 pp. Heist, E. J. (2008) Molecular markers and genetic population structure of pelagic sharks. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Heist, E. J., Musick, J. A. and Graves, J. E. (1996) Genetic population structure of the shortfin mako (Isurus oxyrinchus) inferred from restriction fragment length polymorphism analysis of mitochondrial DNA. Canadian Journal of Fisheries and Aquatic Sciences 53, 583–588. Holdsworth, J. and Saul, P. (2003) New Zealand Billfish and Gamefish Tagging 2001–02. New Zealand Fisheries Assessment Report 2003/15. Ministry of Fisheries, Wellington, New Zealand, 39 pp. Holts, D. B. and Bedford, D. W. (1993) Horizontal and vertical movements of the shortfin mako shark, Isurus oxyrinchus, in the southern California Bight. Australian Journal of Marine and Freshwater Research 44, 901–909. Holts, D. B., Julian, A., Sosa-Nishizaki, O. and Bartoo, N. W. (1998) Pelagic shark fisheries along the west coast of the United States and Baja California, Mexico. In: Proceedings of an International Symposium Held at the 125th Annual Meeting of the American Fisheries Society (ed. R. E. Hueter). Tampa, FL, 30 August 1995. Fisheries Research 39, 115–125. Mejuto, J. (1985) Associated Catches of Sharks, Prionace glauca, Isurus oxyrinchus and Lamna nasus, with NW and N Spanish Longline Fishery, in 1984. ICES C.M. 1985: H42. International Council for the Exploration of the Sea, Copenhagen, Denmark. Mollet, H. F., Cliff, G., Pratt, H. L. and Stevens, J. D. (2000) Reproductive biology of the female shortfin mako Isurus oxyrinchus Rafinesque, 1810, with comments on the embryonic development of lamnoids. Fishery Bulletin 98, 299–318. Mollet, H. F., Testi, A. D., Compagno, L. J. V. and Francis, M. P. (2002) Re-identification of a lamnid shark embryo. Fishery Bulletin 100, 865–875. Muñoz-Chápuli, R., Notarbartolo di Sciara, G., Seret, B. and Stehmann, M. (1993) The Status of the Elasmobranch Fisheries in Europe. IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, 23 pp. Nakano, H. and Honma, M. (1996) Historical CPUE of Pelagic Sharks Caught by Japanese Longline Fishery in the Atlantic Ocean. ICCAT BYC/96/05. ICCAT, Madrid, Spain, 10 pp. Natanson, L. J., Kohler, N. E., Ardizzone, D., Cailliet, G. M., Wintner, S. P. and Mollett, H. F. (2006) Validated age and growth estimates for the shortfin mako, Isurus oxyrinchus, in the North Atlantic Ocean. Environmental Biology of Fishes 77, 367–383. Pepperell, J. G. (1992) Trends in the distribution, species composition and size of sharks caught by gamefish anglers off south-eastern Australia, 1961–90. Australian Journal of Marine and Freshwater Research 43, 213–225. Pratt, H. L. and Casey, J. G. (1983) Age and growth of the shortfin mako, Isurus oxyrinchus, using four methods. Canadian Journal of Fisheries and Aquatic Sciences 40(11), 1944–1957. Snelson Jr., F. F., Roman, B. L. and Burgess, G. H. (2008) The reproductive biology of pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK.

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Stevens, J. D. (1983) Observations on reproduction in the shortfin mako Isurus oxyrinchus. Copeia 1983, 126–130. Stevens, J. D. (1984) Biological observations on sharks caught by sport fishermen off New South Wales. Australian Journal of Marine and Freshwater Research 35, 573–590. Stevens, J. D. (2000) The population status of highly migratory oceanic sharks. In: Getting Ahead of the Curve. Conserving the Pacific Ocean’s Tunas, Swordfish, Billfishes and Sharks (ed. K. Hinman). National Coalition for Marine Conservation, Leesburg, VA. Stevens, J. D. and Wayte, S. S. (1999) A Review of Australia’s Pelagic Shark Resources. Final Report, Project 89/107. Fisheries Research and Development Corporation, Deakin West, Australian Capital Territory, Australia, 64 pp. Stillwell, C. E. and Kohler, N. E. (1982) Food, feeding habits, and daily ration of the shortfin mako (Isurus oxyrinchus) in the Northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 39, 407–414. Yatsu, A. (1995) Zoogeography of the epipelagic fishes in the South Pacific Ocean and the Pacific sector of the Subantarctic, with special reference to the ecological role of slender tuna, Allothunnus fallai. Bulletin of the National Research Institute of Far Seas Fisheries 32, 145 pp.

Chapter 8

The Biology and Ecology of the Salmon Shark, Lamna ditropis Kenneth J. Goldman and John A. Musick

Abstract Salmon sharks (Lamna ditropis) occur only in the North Pacific Ocean. They are the largest apex fish predator in the upper pelagic zone in northern temperate and subarctic Pacific waters, competing with seabirds and marine mammals. This species commonly grows to lengths of 250 cm total length and can weigh at least 220 kg. They segregate by size and sex, and are migratory in nature. Salmon sharks are also endothermic, possessing body temperature elevations as high as 21.2 Cº over ambient water temperature. Currently, the major cause of salmon shark mortality is as bycatch in several pelagic and nearshore fisheries, and the extent of this mortality needs to be better understood to help foster responsible management for this species. Differences in growth rates and age at first maturity between salmon sharks in the eastern and western North Pacific must also be considered, along with movements, migrations, and stock structure, for management to be successful. Key words: salmon shark, Lamma ditropis, Lamnidae, bycatch, endothermy, growth rate, movement, segregation.

Introduction Salmon sharks (Lamna ditropis, Lamnidae) are widely distributed in subarctic and temperate waters of the North Pacific, occurring in both nearshore and oceanic waters (Fig. 8.1) (Strasburg, 1958; Compagno, 1984, 2001). They are currently taken primarily as bycatch in commercial fisheries (mostly in pelagic trawl fisheries) throughout the Pacific, and by sportfishermen in Alaska. A small directed commercial fishery, taking no more than 5,000 sharks per year, occurs off Japan (H. Nakano, personal communication). Lamna ditropis was described as a new species, distinctly different from its congener L. nasus, Bonnaterre 1788 (the porbeagle shark), by Hubbs and Follet (1947). From a southern California specimen, they described the species’ blotched abdomen and the broader and relatively shorter snout as compared to the porbeagle. Other key morphological differences Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Russia

60ç Canada

?

?

? B

45ç

USA

A Japan

30ç

Fig. 8.1 Map showing the geographic range of salmon sharks (Lamna ditropis) in the North Pacific Ocean. (A) Pupping and nursery grounds proposed by Nakano and Nagasawa (1996); (B) pupping and nursery grounds proposed by Goldman (2002 and unpublished data; also see Goldman and Human, 2005). Black oval indicates central California area where numerous young salmon sharks wash up on beaches each spring and summer. Double lines with arrows indicate north–south movements, and the line with question marks indicates current lack of knowledge about trans-Pacific migrations.

include its significantly shorter snout-to-nostril and snout-to-eye lengths, shorter second dorsal and anal fin-to-caudal fin lengths, and slightly different (and weaker) dentition (Nakaya, 1971; Tanaka, 1980). Salmon sharks are heavy thunniform-bodied sharks with a dark bluish-gray to black dorsum changing to a white ventral surface with variable amounts of dark blotches. Other characters include a large first dorsal fin, small second dorsal and anal fins, and a homocercal caudal fin. In addition to strong keels along the caudal peduncle, secondary keels are present along the lower caudal fin base. Tooth counts range from 26 to 30 in the lower jaw and 28 to 30 in the upper jaw (Nagasawa, 1998). While “salmon shark” is the typical common name used for L. ditropis in most countries around the world, the Russian common name translates as “herring shark” (Blagoderov, 1993).

Biology and ecology Adult salmon sharks typically range in size from 180 to 210 cm precaudal length (PCL, where total length (TL)
1.1529  PCL  15.186, from Goldman, 2002, for the eastern North Pacific (ENP); no conversions are given in the literature for salmon sharks in the western North Pacific (WNP)), and can weigh upward of 220 kg. Reported lengths of 260 cm PCL (300 cm TL) and greater, with weights exceeding 450 kg, are unsubstantiated. Length-at-maturity in the WNP has been estimated to occur at approximately 140 cm PCL (at an age of 5 years) for males and between 170 and 180 cm PCL (ages 8–10) for females (Tanaka, 1980), while length-at-maturity in the ENP has been estimated to occur between 125 and 145 cm PCL (ages 3–5) for males and between 160 and 180 cm PCL (ages 6–9) for females (Goldman, 2002; Goldman and Musick, 2006).

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In addition to length- and age-at-maturity, growth rates and weight-at-length of L. ditropis also differ between males and females from the ENP and WNP. Nagasawa (1998, from Tanaka, 1980) stated that maximum age from vertebral analysis for WNP L. ditropis was at least 25 years for males and 17 for females, and that the growth coefficients (k) for males and females were 0.17 and 0.14 year1, respectively. Goldman (2002) and Goldman and Musick (2006) gave maximum ages for ENP L. ditropis (also from vertebral analysis) of 17 years for males and 20 years for females, with growth coefficients of 0.23 and 0.17 year1 for males and females, respectively. Longevity estimates are similar (between 20 and 30 years) for the ENP and WNP, and sharks in both regions attain the same maximum length (approximately 215 cm PCL for females and about 190 cm PCL for males). However, above approximately 140 cm PCL for males and 110 cm PCL for females, salmon sharks in the ENP are of a greater weight-at-length than their same-sex counterparts in the WNP (Goldman, 2002; Goldman and Musick, 2006). The reproductive mode of salmon sharks includes an oophagous stage (Tanaka, 1986, cited in Nagasawa, 1998; Gilmore, 1993). Litter size in the western Pacific is four to five pups and has been reported to be male dominated by a ratio of 2.2:1 (Tanaka, 1980; Nagasawa, 1998). A single pregnant female in the ENP had four pups with a sex ratio of 1:1 (V. F. Gallucci et al., unpublished data). Additionally, in September 2001, a female salmon shark taken in a trawl net just west of Nunavak Island in the Bering Sea contained 41 yolked eggs in her uteri (21 in the left and 20 in the right), with one more found in the right oviducal gland (C. Tribuzio, personal communication). All eggs were about the same size and yolk content; there were no pups. Gestation time throughout the North Pacific has been estimated at 9 months, with mating occurring during the late summer and early fall, and parturition occurring in late spring to early summer (Tanaka, 1980; Nagasawa, 1998; Goldman, 2002; Goldman and Human, 2005; Goldman and Musick, 2006). Size at parturition is between 60 and 65 cm PCL in both the ENP and WNP (Tanaka, 1980; Goldman, 2002; Goldman and Musick, 2006). Salmon sharks are opportunistic feeders, sharing the highest trophic level of the food web in subarctic Pacific waters with marine mammals and seabirds (Brodeur, 1988; Nagasawa, 1998; Goldman and Human, 2005). They feed on a wide variety of prey, including salmon (Oncorhynchus), rockfishes (Sebastes), sablefish (Anoplopoma fimbria), lancetfish (Alepisaurus), daggerteeth (Anotopterus), lumpfishes (Cyclopteridae), sculpins (Cottidae), Atka mackerel (Pleurogrammus), mackerel (Scomber), pollock and tomcod (Gadidae), herring (Clupeidae), spiny dogfish (Squalus acanthias), Tanner crab (Chionocetes), squid, and shrimp (Sano, 1960, 1962; Farquhar, 1963; Okada and Kobayashi, 1968; Hart, 1973; Urquhart, 1981; Compagno, 1984, 2001; Nagasawa, 1998). As with all members of the family Lamnidae, this species is endothermic, retaining heat created by its own oxidative metabolism (Carey et al., 1985; Goldman, 1997; Sepulveda et al., 2004). Body temperatures from moribund or recently dead specimens have shown elevations (over water temperature) of 8–11 Cº in smaller specimens and up to 13.6 Cº in larger specimens (Smith and Rhodes, 1983; Anderson and Goldman, 2001). Body core temperature in free-swimming salmon sharks appears to be maintained regardless of ambient temperature conditions and can exceed ambient water temperature by as much as 21.2 Cº (Goldman, 2002; Goldman et al., 2004).

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Distribution and movements Salmon sharks occur throughout the North Pacific, most commonly ranging from 65ºN latitude to 35ºN in the west and to 30ºN in the east (Fig. 8.1) (Compagno, 1984; Nagasawa, 1998; Goldman and Human, 2005). They are most concentrated between 50ºN and 60ºN latitude, with northern and southern range extremes of approximately 70ºN and 10ºN latitude (Neave and Hanavan, 1960; Blagoderov, 1994; Nakano and Nagasawa, 1996; Nagasawa, 1998), and occur individually and in large aggregations. Vertical distribution ranges from the surface to at least 150 m. They are found in sea-surface temperatures of 9–16 C°, but occur in waters as cold as 52°C and as warm as 18 C°. There appear to be two separate salmon shark pupping and nursery grounds in the North Pacific. From captures of young sharks and a few pregnant females, one has been proposed to exist along the transitional boundary of the subarctic and central Pacific currents (Nakano and Nagasawa, 1996). Another pupping and nursery ground appears to range from the Alaska–Canada border to the northern end of Baja California, Mexico, based on a few captures and numerous young salmon sharks (ages 0–5) that wash up on beaches each year along the western United States (Fig. 8.1) (K. J. Goldman, unpublished data). Like many shark species, salmon sharks segregate by size and sex. However, a remarkable sex ratio difference exists across the North Pacific basin. The western side is male dominated and the eastern side is female dominated, and dominance increases with latitude (Table 8.1). Larger sharks range farther north than smaller individuals, and southern catches generally occur in deeper waters (Nagasawa, 1998; K. J. Goldman and J. A. Musick, unpublished data). Size segregation appears to be quite specific, as catches from aggregations in Alaska waters are typically within 10–15 cm of each other (K. J. Goldman et al., unpublished data). The migratory nature of salmon sharks in the western and central North Pacific was first described over 60 years ago (Iino, 1939). Subsequent analysis of Japanese longline and Russian trawl data supports Iino’s (1939) suggestion of a northern migration in spring and a southern migration in autumn (Tanaka, 1980; Gorbatenko and Cheblukova, 1990; Blagoderov, 1994; Nakano and Nagasawa, 1994, 1996). Data from tagging with streamer and satellite tags (see below), as well as from salmon and squid fisheries bycatch, suggest that a similar north–south seasonal migration occurs in the ENP; however, salmon sharks are present in the Gulf of Alaska and Prince William Sound throughout the year (Goldman and Human, 2005; Weng et al., 2005). Longline and bycatch data from oceanic Table 8.1 Sexual segregation in salmon sharks (Lamna ditropis) across the Pacific basin and with increasing latitude. Western North Pacifica

Eastern North Pacificb

Male dominated 40–45ºN
50–60% 46–50ºN
70–90% 52ºN
90%

Female dominated 35–40ºN
65–70% 40–50ºN
78% 50ºN
85–92%

a

Data from Sano (1962) and Nagasawa (1998). Data from Goldman (2002).

b

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salmon surveys between 1981 and 1991 also indicate that a northeasterly movement across the North Pacific basin may take place beginning in April and peaking in July (Tanaka, 1980; Nakano and Nagasawa, 1996). With the high percentage of females in the ENP and males in the WNP, the movement of males across the Pacific basin may help create mating aggregations in the Gulf of Alaska and adjacent waters during late July through August, when males are more commonly found in Alaskan waters (Goldman and Human, 2005; K. J. Goldman and J. A. Musick, unpublished data). Tagging studies were conducted in the WNP by the Japan Marine Fishery Resource Research Center during 1979 and 1980, and a total of 134 sharks were tagged (Makihara et al., 1980, and Yamaki and Maruyama, 1981, cited in Nagasawa, 1998). One recapture had moved roughly 200 km (from off of Japan closer to shore) after 5 months at large and had grown 5 cm PCL, but no lengths at tagging and recapture were reported (Nagasawa, 1998). A tagging program in the ENP instituted in 1998 by the Alaska Department of Fish and Game (ADF&G) has tagged over 675 sharks to date and had 26 recaptures (S. Meyer and C. Stock, personal communication). Several tagged sharks have been resighted with algae-covered tags, indicating they have been at large for some time. The longest time at large between tag and recapture has been 6 years. The longest-distance tag recapture was from an individual tagged in eastern Prince William Sound (60º40N, 146º12W) on July 26, 1999, which was recaptured by a commercial salmon fisherman 49 days later southeast of Prince of Wales Island at Chasina Point, in southeast Alaska (55º20N, 132º00W), a distance of over 1,045 km (Fig. 8.2). The shark was re-released in good condition

Prince William Sound

Tagged 26 July 1999

Cook Inlet

Tagged 17 July 1998

Recaptured 12 September 1999


Video recapture; 24 July 1998
Alaska Department of Fish and Game streamer tag

Fig. 8.2 Longest-distance tag recaptures in south-central and southeast Alaska (Alaska Department of Fish and Game).

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(C. Stock, personal communication). Pop-up satellite tags recently deployed in Prince William Sound show wide-ranging movements throughout the ENP (Weng et al., 2005). While some movements were in a westerly direction toward the outer chain of Alaskan islands, no tagged sharks have moved across the North Pacific to the western side (none has moved across longitude 170ºW). Some sharks have ranged as far as southern California and Hawaii, and some individuals have made repeated annual migrations from Alaska to waters off California; still others have overwintered in Alaska waters (Weng et al., 2005). Recent acoustic telemetry tracks along with several years of observation indicate that there is short-term site fidelity to particular areas in the Gulf of Alaska and Prince William Sound (K. J. Goldman et al., unpublished data). Of the several resightings of tagged sharks in the last 10 years, most have been in the general area where they were tagged. One in particular deserves mention. Six salmon sharks were tagged with ADF&G streamer tags on July 17, 1998, in Montague Straits at the western end of Prince William Sound. One of these sharks was inadvertently tagged in the lower part of its first dorsal fin. On July 24, 1998, two tagged sharks were sighted with an underwater video camera in Resurrection Bay, Alaska, and one of them had a tag through its first dorsal fin (S. Anderson, personal communication) (Fig. 8.2). Since no other salmon sharks were tagged at that point in time, these animals were almost certainly two of the ones tagged in Montague Straits. These sharks traveled a distance of approximately 110 km in 7 days, and their presence together suggests that aggregations (or individuals within an aggregation) may travel as groups. The stock structure of salmon sharks is not well understood at this time. Nagasawa (1998) stated that salmon sharks from the western and central North Pacific appear to constitute a single stock; however, this assertion is based on small amounts of data on annual migrations and has no genetic support (Sano, 1962; Tanaka, 1980; Blagoderov, 1994).

Threats and status Historical records of commercial catch and bycatch of salmon sharks are sparse. The Japanese commercial catch was reported to the UN Food and Agriculture Organization between 1952 and 1965, totaling 110.4 metric tons (t), with 40.1 t being the highest amount taken in any single year (Compagno, 1990). The current fishing mortality on salmon sharks comes mainly from being taken as bycatch in purse-seine fisheries (e.g., for salmon), but they are also taken in longline fisheries for halibut and sablefish. There is a small amount of directed commercial and sportfishing occurring off Japan and in Alaska waters, respectively. Historically, salmon sharks were commonly caught in gill nets set for salmon (Oncorhynchus spp.) and flying squid (Ommastrephes), primarily by Canadian, Japanese, and Russian fisheries, with smaller numbers taken by Taiwanese and North Korean fisheries (Robinson and Jamieson, 1984; McKinnell and Waddell, 1993; Blagoderov, 1994; Nakano and Nagasawa, 1996). On the basis of the number of boats, average number of sets, and the average catch per unit effort (CPUE) reported in Robinson and Jamieson (1984), flying squid fisheries may have taken between 105,000 and 155,000 salmon sharks as bycatch over a 4-month period each year (Goldman and Human, 2005). With the

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elimination of open ocean drift-net fishing and the cessation of the Japanese open ocean salmon fishery, there is now less salmon shark bycatch in the open North Pacific and the population may have rebounded to near previous levels (Yatsu et al., 1993; Goldman, 2002). Additionally, the most recent demographic analysis supports the contention that salmon shark populations in the ENP and WNP are stable at this time (Goldman, 2002). However, salmon sharks are still taken in US waters (particularly the Gulf of Alaska and Prince William Sound) as bycatch in trawl, gill-net, and seine fisheries, but this bycatch has been poorly documented (Camhi, 1999), and salmon shark bycatch in fisheries of other countries is not reported. There is a great need to document the bycatch in US and federal waters in order to foster responsible management of this species, as well as to obtain detailed catch and bycatch records from the WNP. Sharks are currently listed in the Federal Groundfish Management Plans for the Gulf of Alaska, Bering Sea, and Aleutian Islands as “other species” and are allowed as bycatch. This categorization may change in the near future and sharks may be managed separately from the other species group. They are included in the commercial bycatch TAC (total allowable catch) for Alaska federal waters, but what percentage of this bycatch is salmon shark (versus spiny dogfish and sleeper shark, Somniosus pacificus) is unknown (W. Bechtol, personal communication), although documentation by species is improving. The North Pacific Fishery Management Council is currently considering closure of directed commercial fishing for sharks in federal waters as no federal management plan exists specifically for sharks in the Gulf of Alaska, Aleutians, and Bering Sea (J. DiCosimo, personal communication). Commercial fishing for sharks in Alaska state waters has been illegal since 1998. Sportfishing regulations in Alaska are two sharks per person per year, and one in possession at any time (one per day). The state extended the sportfishing regulations to include the exclusive economic zone (EEZ, to 200 miles), as the federal management plans do not currently cover sportfishing. No abundance estimates are available for salmon sharks in the ENP. Estimates of minimum stock size for the western and central North Pacific range from 1.66  106 to 2.19  106 (H. Shimida and H. Nakano, unpublished data, cited in Nagasawa, 1998). These sharks are believed to be the major ocean predator of salmonids, and one estimate has them consuming between 113,000 and 226,000 t per summer, which would translate to between 73 million and 146 million individual salmon (Nagasawa, 1998). Unfortunately, the derivations of these abundance and consumption estimates were not presented in detail. Current research is beginning to assess local densities of salmon sharks and to examine the genetic stock structure in the ENP and WNP in order to foster responsible management of the species. The variability in growth rates and strong sexual segregation across the North Pacific basin, and the unknown rate of current bycatch, are all complicating factors for successful salmon shark management.

Acknowledgments We thank Merry Camhi and Ellen Pikitch for organizing the International Pelagic Shark Workshop in Pacific Grove, California, and for requesting this resulting chapter. Thanks to Scot Anderson, Kari Anderson, Bob Candopoulos, many crew members and

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customers aboard the F.V. Legend, Jane DiCosimo, Barbara Block, Jose Castro, and Bill Steffen for field help and logistical support. Great thanks go to Bill Bechtol, Scott Meyer, Charlie Stock, Matt Miller, Charlie Trowbridge, Doug Vincent-Lang, and Mike Bethe (Alaska Department of Fish and Game) for their staunch support of salmon shark research in Alaska, and to Gary Stevens and Kim Fisher for reporting the ADF&G tagged shark. Special thanks from K.J.G. to Consuelo Goldman for her never-ending personal support, and to Hideki Nakano for numerous discussions on salmon shark biology.

References Anderson, S. D. and Goldman, K. J. (2001) Temperature measurements from salmon sharks, Lamna ditropis, in Alaskan waters. Copeia 2001(3), 794–796. Blagoderov, A. I. (1993) Seasonal distribution and some notes on the biology of herring shark (Lamna ditropis) in the northwestern Pacific Ocean. Voprosy Ikhtiologii 33(5), 715–719 (in Russian). Blagoderov, A. I. (1994) Seasonal distribution and some notes on the biology of salmon shark (Lamna ditropis) in the northwestern Pacific Ocean. Journal of Ichthyology 34(2), 115–121. Brodeur, R. D. (1988) Zoogeography and trophic ecology of the dominant epipelagic fishes in the northern Pacific. In: The Biology of the Subarctic Pacific (eds. T. Nemoto and W. G. Percy). Bulletin of the Ocean Research Institute, No. 26 (Part II). University of Tokyo, Tokyo, Japan, pp. 1–27. Camhi, M. (1999) Sharks on the Line II: An Analysis of Pacific State Shark Fisheries. National Audubon Society, Islip, NY, 114 pp. Carey, F. G., Casey, J. G., Pratt, H. L., Urquhart, D. and McCosker, J. E. (1985) Temperature, heat production, and heat exchange in lamnid sharks. Memoirs of the Southern California Academy of Sciences 9, 92–108. Compagno, L. J. V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 1. Hexanchiformes to Lamniformes. FAO Fisheries Synopsis No. 125. FAO, Rome, Italy, pp. 1–249. Compagno, L. J. V. (1990) Shark exploitation and conservation. In: Elasmobranchs As Living Resources: Advances in Biology, Ecology, Systematics, and the Status of the Fisheries. NOAA Technical Report NMFS 90. NOAA/NMFS, Silver Spring, MD, pp. 391–414. Compagno, L. J. V. (2001) FAO Species Catalogue for Fishery Purposes. No. 1. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Vol. 2. Bullhead, Mackerel and Carpet Sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO, Rome, Italy, 269 pp. Farquhar, G. B. (1963) Sharks of the Family Lamnidae. Technical Report TR-157. US Naval Oceanographic Office, Stennis Space Center, MS, 22 pp. Gilmore, R. G. (1993) Reproductive biology of lamnoid sharks. Environmental Biology of Fishes 38, 95–114. Goldman, K. J. (1997) Regulation of body temperature in the white shark, Carcharodon carcharias. Journal of Comparative Physiology B 167(6), 423–429. Goldman, K. J. (2002) Aspects of Age, Growth, Demographics and Thermal Biology of Two Lamniform Shark Species. Ph.D. dissertation, College of William and Mary, School of Marine Science, Virginia Institute of Marine Science, Gloucester Point, VA, 220 pp. Goldman, K. J. and Human, B. (2005) Salmon shark, Lamna ditropis Hubbs and Follett, 1947. In: Sharks, Rays and Chimaeras: The Status of the Chondrichthyan Fishes (eds. S. L. Fowler et al.).

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IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 260–262. Goldman, K. J. and Musick, J. A. (2006) Growth and maturity of salmon sharks in the eastern and western North Pacific, with comments on back-calculation methods. Fishery Bulletin 104, 278–292. Goldman, K. J., Anderson, S. D., Latour, R. J. and Musick, J. A. (2004) Homeothermy in adult salmon sharks, Lamna ditropis. Environmental Biology of Fishes 71(4), 403–411. Gorbatenko, K. M. and Cheblukova, L. V. (1990) Environment conditions and fish species composition in the epipelagic zone of the Okhotsk Sea during summer. Journal of Ichthyology 30, 89–100. Hart, J. L. (1973) Pacific fishes of Canada. Bulletin of the Fisheries Research Board of Canada 180, 36–37. Hubbs, C. L. and Follett, W. I. (1947) Lamna ditropis, new species, the salmon shark of the North Pacific. Copeia 1947(3), 194. Iino, R. (1939) Migration of salmon sharks. Suisan Kenkyu-shi 34, 171–173 (in Japanese). Makihara, M., Nakano, T. and Tanaka, S. (1980) Report of New Shark Resource Exploitation Survey in the Fiscal Year 1979 (North Pacific Ocean). Japan Marine Fishery Resource Research Center, Tokyo, Japan, 222 pp. (in Japanese). McKinnell, S. and Waddell, B. (1993) Associations of species caught in the Japanese large scale pelagic squid driftnet fishery in the central North Pacific Ocean: 1988–1990. International North Pacific Fisheries Commission Bulletin 53(2), 91–109. Nagasawa, K. (1998) Predation by salmon sharks (Lamna ditropis) on Pacific salmon (Oncorhynchus spp.) in the North Pacific Ocean. Bulletin of the North Pacific Anadromous Fish Commission 1, 419–433. Nakano, H. and Nagasawa, K. (1994) Distribution of the salmon shark (Lamna ditropis) in the North Pacific Ocean and Bering Sea. In: Salmon Report Series, No. 37. National Research Institute of Far Seas Fisheries, Shimizu, Japan, pp. 226–237. Nakano, H. and Nagasawa, K. (1996) Distribution of pelagic elasmobranchs caught by salmon research gillnets in the North Pacific. Fisheries Science 62(5), 860–865. Nakaya, K. (1971) Descriptive notes on a porbeagle, Lamna nasus, from Argentine waters, compared with the North Pacific salmon shark, Lamna ditropis. Bulletin of the Faculty of Fisheries, Hokkaido University 21(4), 269–279. Neave, F. and Hanavan, M. G. (1960). Seasonal distribution of some epipelagic fishes in the Gulf of Alaska region. Journal of the Fisheries Research Board of Canada 17(2), 221–233. Okada, S. and Kobayashi, K. (1968) Colored Illustrations of Pelagic and Bottom Fishes in the Bering Sea. Japan Fisheries Research Consortium Association, Tokyo, Japan, 179 pp. (in Japanese). Robinson, S. M. C. and Jamieson, G. S. (1984) Report on a Canadian Commercial Fishery for Flying Squid Using Drifting Gill Nets off the Coast of British Columbia. Canadian Industry Report of Fisheries and Aquatic Science No. 150. Department of Fisheries and Oceans, Nanaimo, British Columbia, Canada, 25 pp. Sano, O. (1960) The investigation of salmon sharks as a predator on salmon in the North Pacific, 1959. Bulletin of the Hokkaido Regional Fisheries Research Laboratory, Fisheries Agency 22, 68–82 (in Japanese). Sano, O. (1962) The investigation of salmon sharks as a predator on salmon in the North Pacific, 1960. Bulletin of the Hokkaido Regional Fisheries Research Laboratory, Fisheries Agency 24, 148–162 (in Japanese). Sepulveda, C. A., Kohin, S., Chan, C., Vetter, R. and Graham, J. B. (2004) Movement patterns, depth preferences, and stomach temperatures of free-swimming juvenile mako sharks, Isurus oxyrinchus, in the Southern California Bight. Marine Biology 145, 191–199.

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Smith, R. L. and Rhodes, D. (1983) Body temperature of the salmon shark, Lamna ditropis. Journal of the Marine Biological Association of the United Kingdom 63, 243–244. Strasburg, D. W. (1958) Distribution, abundance, and habits of pelagic sharks in the central Pacific Ocean. US Fisheries Bulletin 58, 335–361. Tanaka, S. (1980) Biological investigation of Lamna ditropis in the north-western waters of the North Pacific. In: Report of Investigation on Sharks As a New Marine Resource (1979). Japan Marine Fishery Resource Research Center, Tokyo, Japan (English abstract). Tanaka, S. (1986) Sharks. Iden (Heredity) 40, 19–22 (in Japanese). Urquhart, D. L. (1981) The North Pacific salmon shark. Sea Frontiers 27(6), 361–363. Weng, K. C., Castilho, P. C., Morrissette, J. M., Landeira-Fernandez, A. M., Holts, D. B., Schallert, R. J., Goldman, K. J. and Block, B. A. (2005) Satellite tagging and cardiac physiology reveal niche expansion in salmon sharks. Science 310, 104–106. Yamaki, K. and Maruyama, T. (1981) Report of New Shark Resource Exploitation Survey in the Fiscal Year 1980 (North Pacific Ocean). Japan Marine Fishery Resource Research Center, Tokyo, Japan, 133 pp. (in Japanese). Yatsu, A., Hiramatsu, K. and Hayase, S. (1993) Outline of the Japanese squid driftnet fishery with notes on the by-catch. In: Symposium on Biology, Distribution and Stock Assessment of Species Caught in the High Seas Driftnet Fisheries in the North Pacific Ocean (eds. J. Ito, W. Shaw and R. L. Burgener). Tokyo, Japan, 4–6 November 1991. International North Pacific Fisheries Commission Bulletin 53, 5 pp.

Chapter 9

The Biology and Ecology of the Porbeagle Shark, Lamna nasus Malcolm P. Francis, Lisa J. Natanson and Steven E. Campana

Abstract Information on the biology, ecology, and fisheries of porbeagle sharks (Lamna nasus) is reviewed to assess biological and population parameters that are relevant to stock assessment, and to identify gaps in our knowledge. Separate porbeagle stocks occur in the Northwest and Northeast Atlantic, but stock identity is poorly understood in the Southern Hemisphere. Porbeagles are born at 58–67 cm fork length (FL). Length at maturity is lower for Southwest Pacific males and females (about 140–150 and 170–180 cm FL, respectively) than for North Atlantic males and females (166 and 208 cm FL). Ages at 50% maturity for North Atlantic males and females are 8 and 13 years, respectively. Porbeagles recruit to commercial fisheries in both hemispheres during their first year. North Atlantic males and females reach at least 253 and 302 cm FL, respectively, and longevity exceeds 26 years. Age at maturity and longevity in the Southwest Pacific are unknown. Growth is almost linear, and similar for both sexes, for about 8 years, after which females grow faster. The rate of natural mortality for the Northwest Atlantic is 0.10 for immature sharks, rising to 0.15–0.20 for mature sharks. The gestation period is 8–9 months and the length of the female reproductive cycle may be about 1 year. Mean litter size is 3.7–4.0 embryos, and the embryonic sex ratio is 1:1. Porbeagle sharks are vulnerable to overfishing. Directed fisheries in the Northwest Atlantic are now restricted by catch quotas, but stock biomass declined to about 10–20% of virgin biomass before restrictive quotas were introduced. In the Southern Hemisphere, porbeagles are taken mainly as bycatch in tuna longline fisheries; no biomass estimates or stock assessments are available. The low productivity of porbeagles and their history of overfishing indicate that sustainable yields will be low. Key words: porbeagle, Lamna nasus, Lamnidae, growth, maturity, longevity, mortality, reproduction, stock status.

Introduction Porbeagles (Lamna nasus, Lamnidae) are thermoregulating sharks that inhabit temperate, subarctic, and subantarctic waters. They live mainly in the open ocean and over continental Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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shelves, but also enter coastal waters. Porbeagles have proven to be vulnerable to overfishing in the Northwest Atlantic: A target longline fishery in the 1960s lasted only 6 years before collapsing. This fishery was revived by Canadian and US vessels in the 1990s, but catch levels during the last decade appear to be unsustainable (Campana et al., 2002a, 2008). In the Southern Hemisphere, porbeagles have not been targeted, but they are frequently taken as bycatch in tuna longline fisheries (Francis et al., 2001; Ayers et al., 2004). The history of the Northwest Atlantic fishery demonstrates a need for cautious, assessment-based management of porbeagles. Until recently, information on the biology of porbeagles was sparse. Aasen (1961, 1963) conducted pioneering studies on porbeagle biology in the Northwest Atlantic, but there was little increase in knowledge until dedicated studies were made in the North Atlantic and Southwest Pacific Oceans beginning in the late 1980s (Gauld, 1989; Francis and Stevens, 2000; Francis et al., 2001; Campana et al., 2002a, b; Jensen et al., 2002; Joyce et al., 2002; Natanson et al., 2002; Francis and Duffy, 2005). This chapter reviews the available biological and fishery information on porbeagles, presents the best available estimates of biological and population parameters that are relevant to stock assessment, and identifies data gaps that need to be addressed before detailed assessment is possible.

Distribution, movements, and stock structure Porbeagles live mainly in the latitudinal bands 30–50ºS and 30–70ºN (Last and Stevens, 1994; Yatsu, 1995; Francis and Stevens, 2000). They occur in the North Atlantic Ocean and in a circumglobal band in the Southern Hemisphere. Porbeagles are absent from the North Pacific Ocean, where they are replaced by the closely related salmon shark (Lamna ditropis, Lamnidae). In the South Pacific Ocean, porbeagles are caught north of 30ºS only in winter–spring; in summer they are not found north of about 35ºS (Yatsu, 1995). Off the east coast of Australia, porbeagles enter subtropical waters (to 23º44
S) in winter. They appear to penetrate farther south during summer and autumn (Yatsu, 1995), and are found near many of the subantarctic islands in the Indian and Southwest Pacific Oceans (Francis and Stevens, 2000). The temperature range inhabited by porbeagles in the Southern Hemisphere is about 1–23ºC, with abundance declining above about 19ºC (Svetlov, 1978; Stevens et al., 1983; Yatsu, 1995; Francis and Stevens, 2000). Most Northwest Atlantic porbeagles are caught at temperatures between –1ºC and 15ºC, with a mean of 7–8ºC at the depth of the fishing gear (Campana and Joyce, 2004). In the North Atlantic, porbeagle abundance varies seasonally and spatially (Aasen, 1961, 1963; Templeman, 1963; Mejuto and Garcés, 1984; Mejuto, 1985; Gauld, 1989). Off North America, porbeagles move north along the coast in spring and early summer and spend late summer and fall at about 46–48ºN; the return migration occurs in the late fall (Campana et al., 1999). In the Northwest Atlantic, several studies found that most tagged sharks move short to moderate distances (up to 1,500 km) along continental shelves, though one moved about 1,800 km off the shelf into the mid-Atlantic Ocean (Kohler et al., 1998; O’Boyle

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et al., 1998; Campana et al., 1999). Sharks tagged off southern England were mainly recaptured between Denmark and France, with one shark moving 2,370 km to northern Norway (Stevens, 1976, 1990). Only one tagged shark has crossed the Atlantic: It traveled 4,260 km from southwest Ireland to 52ºW off eastern Canada (Kohler and Turner, 2001; P. Green, personal communication). Thus porbeagles from the Northwest and Northeast Atlantic appear to form two distinct stocks (Campana et al., 1999). Stock structure in the Southern Hemisphere is unknown, but if movements are similar in scale to those in the North Atlantic, there would be several stocks. There have been no genetic studies to determine the number of porbeagle stocks, but based on the disjunct (antitropical) geographic distribution, North Atlantic porbeagles are probably reproductively isolated from Southern Hemisphere porbeagles.

Biology and ecology Length–length and length–weight relationships In this chapter, we use straight-line fork length (FL) for all measurements except where otherwise stated. Literature reports based on other measurement methods (mainly FL measured over the body and total length, TL) were converted to straight-line FL. Length– length and length–weight relationships are given in Table 9.1. Other length–length regressions were provided by Aasen (1963) and Campana et al. (1999). Gauld (1989) found significant differences in weight between males and females longer than 180 cm. Other length–weight relationships based on smaller sample sizes have been published for the North Atlantic (Aasen, 1961; Mejuto and Garcés, 1984; Stevens, 1990; Ellis and Shackley, 1995; Kohler et al., 1995).

Length at birth and maturity The length at birth is 58–67 cm in the Southwest Pacific (Francis and Stevens, 2000) and is probably similar in the North Atlantic (Gauld, 1989; Jensen et al., 2002). In the Northwest Atlantic, females mature at 200–219 cm, and 50% are mature by 208 cm (Jensen et al., 2002). Males mature at 155–177 cm, and the length at 50% maturity is 166 cm (Jensen et al., 2002). Off New Zealand, males mature at about 140–150 cm and females at 170–180 cm (Francis and Duffy, 2005). Thus both sexes mature at substantially smaller lengths in the Southwest Pacific than in the Northwest Atlantic.

Growth, maturity, and recruitment Age and growth have been comprehensively studied in the Northwest Atlantic, and age estimation has been validated up to 26 years (Campana et al., 2002b; Natanson et al., 2002). Growth in both sexes is similar up to the age of maturity, whereupon growth slows. Because females mature later than males, the growth curves diverge (Table 9.1). Males mature at 6–10 years, with 50% mature at 8 years, and females mature at 12–16 years,

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Table 9.1 Summary of porbeagle biological parameters.* Parameter

Southwest Pacific Ocean Source

Stock structure Length–length relationships (cm)

? FL–0.567  0.881 TL TL4.165  1.098 FL PL–1.366  0.907 FL FL1.990  1.098 PL

Length–weight relationship (kg, cm)

F  M: W8.91  106 FL3.128 ( juveniles  150 cm)

1

Length at birth (cm) Length at maturity (cm)

58–67 FL F: 170–180 FL M: 140–150 FL NZ: FL  66.5  19.8 age Australia: FL  65.4  16.1 age (juveniles  150 cm) F: ? M: ? 0–1 F: 208 FL M: 204 FL ? ? 8–9 1 3.75 3.75 FM

1, 2 3

Growth

Median age at maturity (year) Age at recruitment (year) Maximum length (cm) Longevity (years) Natural mortality (year–1) Gestation period (months) Reproductive cycle (year) Mean litter size Annual fecundity Embryonic sex ratio

1

1

1 1, 2

1, 2 1 1, 2 1, 2 1, 2

Value

Source

NW Atlantic, NE Atlantic CFL0.99  0.885 CTL CTL1.12 CFL CPL –1.36  0.89 CFL CFL1.7  1.12 CPL FL0.90  0.95 CFL FM: W  5  105 CFL2.713 F: W  3  104 TL2.357 M: W  1.9  103 TL2.008 Similar to SW Pacific F: 200–219 FL; 50% 208 FL M: 155–177 FL; 50% 166 FL F  M: CFL  289.4(1–e0.066 (t  6.06)) F: CFL  309.8(1–e–0.061 (t  5.90)) M: CFL  257.7(1–e–0.080 (t  5.78)) F: 13 M: 8 0–1 F: 278 FL; M: 253 FL F: 302 FL; M: 250 FL 26 0.10–0.20 8–9 1? 3.7–4.0 ⬃3.7–4.0? FM

4 4

9 4 5 5 1, 6 6 6 7

6, 7 6, 7 8 5 9 10 4, 8 1, 6 1, 6 5, 6 5, 6 6

*?: unknown; FL: fork length; TL: total length; PL: precaudal length; CFL: curved fork length (over the curve of the body); CTL: curved total length; CPL: curved precaudal length; W: weight; M: males; F: females. Sources: 1: Francis and Stevens (2000); 2: M. P. Francis, unpublished data; 3: Francis and Duffy (2005); 4: Campana et al. (1999); 5: Gauld (1989); 6: Jensen et al. (2002); 7: Natanson et al. (2002); 8: Campana et al. (2001); 9: S. E. Campana, unpublished data; 10: Campana et al. (2002a).

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Value

North Atlantic Ocean

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with 50% mature by 13 years (Jensen et al., 2002; Natanson et al., 2002). In the Southwest Pacific, juveniles grow 16–20 cm/year for 4–5 years and reach 110–125 cm after 3 years (Francis and Stevens, 2000). Porbeagles recruit to commercial fisheries during their first year, and much of the commercial catch is immature (Campana et al., 2001; Francis et al., 2001; Ayers et al., 2004).

Maximum length, longevity, and natural mortality Lengths of 253 and 278 cm for males and females, respectively, are the largest reliable measurements from the Northeast Atlantic (Gauld, 1989). In the Northwest Atlantic, the greatest known lengths are 250 cm (males) and 302 cm (females) (S. E. Campana, unpublished data). Thus females grow larger than males, and the maximum reported length is 302 cm (335 cm TL). In the Southwest Pacific, the largest male and female porbeagles recorded were 236 and 208 cm, respectively (Francis and Stevens, 2000; Ayers et al., 2004; M. Francis, unpublished data). However, only four males exceeding 204 cm have been recorded in the region and they were 220–236 cm long, so these outliers may have been incorrectly measured or identified. If so, the maximum known lengths for males and females are 204 and 208 cm, respectively. Thus Southwest Pacific porbeagles appear to reach considerably smaller maximum lengths than North Atlantic porbeagles, and there is little difference between the sexes. The greatest known age is 26 years for a 251-cm porbeagle (Campana et al., 2002a), but this likely underestimates longevity because the population had been fished. Indirect methods based on the von Bertalanffy growth curve and estimates of natural mortality indicate they may live for more than 40 years (Natanson et al., 2002). The natural mortality rate has been estimated as 0.10 for immature porbeagles of both sexes, rising to 0.15 for mature males and about 0.20 for mature females (Campana et al., 1999, 2001).

Length, age, and sex composition Porbeagles appear to segregate by size and sex. Off Spain, twice as many males as females are caught (Mejuto, 1985), whereas 30% more females are caught off Scotland (Gauld, 1989). In the Bristol Channel, United Kingdom, the size composition is skewed toward smaller, presumably immature individuals and the population is dominated by males (Ellis and Shackley, 1995). In the Northwest Atlantic there is a marked segregation by sex in individual catches, but the overall sex ratio is balanced (Aasen, 1963; O’Boyle et al., 1998). There is a strong seasonal shift in size composition: Spring catches are dominated by small, immature sharks, while the fall fishery farther to the north takes mainly larger, mature sharks (Campana et al., 1999). In the Southwest Pacific, catches are dominated by immature sharks (Francis et al., 2001; Ayers et al., 2004). The size and sex distributions of both sexes are comparable up to about 150 cm, but larger individuals are predominantly male; few mature females are caught. Regional differences in length composition suggest segregation by size (Francis and Stevens, 2000).

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Reproduction Porbeagles are aplacental viviparous and oophagous (Francis and Stevens, 2000; Jensen et al., 2002). The embryonic growth rate is 8 cm per month, and the gestation period is about 8–9 months, though the high variability and uneven temporal distribution of the data mean that the latter estimate is uncertain (Francis and Stevens, 2000; Jensen et al., 2002). In the Northwest Atlantic, all females sampled in winter were pregnant, suggesting that there is no extended resting period between pregnancies, and that the female reproductive cycle lasts for 1 year (Jensen et al., 2002). Litter size is usually four embryos, but ranges from one to five (Bigelow and Schroeder, 1948; Gauld, 1989; Francis and Stevens, 2000; Jensen et al., 2002). Mean litter sizes in the Southwest Pacific, Northeast Atlantic, and Northwest Atlantic were 3.75, 3.70, and 4.0, respectively (Gauld, 1989; Francis and Stevens, 2000; Jensen et al., 2002; M. P. Francis, unpublished data). If the reproductive cycle lasts for 1 year, annual fecundity would be about 3.7–4.0 young per female. The sex ratio of embryos is not significantly different from one (Francis and Stevens, 2000; Jensen et al., 2002).

Diet Porbeagles are active predators of fish and cephalopods (Gauld, 1989; Ellis and Shackley, 1995). In the Northwest Atlantic, pelagic fish and squid dominate the diet in deep water, and pelagic and demersal fish are consumed in shallow water (Joyce et al., 2002). Gastropods, crabs, and debris have also been observed in stomachs.

Threats and status Fisheries Porbeagles have been fished since at least the 1920s to supply markets with fresh and dried flesh, oil, fish meal, and fins. Global catches peaked at more than 9,000 metric tons (t) in the 1960s, declining to 1,300–2,600 t in the 1990s as both sides of the Atlantic became overfished (Myklevoll, 1989; O’Boyle et al., 1998; Campana et al., 1999, 2001, 2008). Porbeagles are taken in the Atlantic primarily by a directed pelagic longline fishery, although there is some bycatch from bottom trawls, handlines, and gill nets (Gauld, 1989; Myklevoll, 1989; Campana et al., 1999). In contrast, most of the catch in the Southern Hemisphere is bycatch from tuna longline fleets operating in the South Pacific and southern Indian Oceans (Francis et al., 2001; Ayers et al., 2004; J. D. Stevens, personal communication). Management restrictions on porbeagle catches vary depending on the area and regulating country. Total catches by the European Union in the Northeast Atlantic are now regulated, and strict quotas have been implemented in the Northwest Atlantic. In addition, the mating aggregations in the Canadian portion of the Northwest Atlantic have been protected by a time and area closure. Catch quotas were introduced in New Zealand in 2004, and there is a general finning ban in Australia. There is a recreational fishery for porbeagles on both sides of the North Atlantic, but catches are small. The US recreational fishery is regulated by a bag limit.

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Stock status With the exception of the Northwest Atlantic stock, little is known about stock status. Myklevoll (1989) reported that directed catch rates by the Norwegian fleet in European waters were poor after 1960, prompting the shift of the fishery to the then-unexploited population in the Northwest Atlantic. No trends in abundance were noted in Scottish waters, although Gauld (1989) concluded that only a small portion of the stock area was fished by Scottish vessels. Reported catches from the Northeast Atlantic were low in the 1990s compared to earlier years (Campana et al., 1999, 2001, 2008), suggesting that relative abundance was low. In the Northwest Atlantic, stock status has been assessed using annual trends in length composition, total mortality, and commercial catch per unit effort (CPUE), and Petersen analysis of tag recaptures (Campana et al., 1999, 2001, 2002a). The median length of sharks in the offshore commercial fishery has declined from more than 200 cm to about 140 cm since 1960. By 2000, the standardized CPUE of mature porbeagles had declined to 10% of its 1992 level. Three independent measures of fishing mortality were all above a level that would maintain the stock size at current levels, or allow it to recover. The 2000 biomass was 10–20% of estimated virgin biomass. In 2002 the Canadian quota was reduced to 25% of recent quotas in an attempt to make the catch sustainable. In 1999, the United States separated porbeagles from the general pelagic shark quota in an effort to manage this species independently. In the South Pacific, the likelihood of unreported landings, the absence of adequate CPUE data, and the presumably large geographic range of the stock complicate any attempt at assessing population status (Francis et al., 2001; Ayers et al., 2004). Unstandardized CPUE indices from 1993 are available for New Zealand waters, but the relative rarity of mature individuals in the catch suggests that they are not reliable measures of overall stock abundance (Ayers et al., 2004).

Acknowledgments This study was partly funded by the New Zealand Ministry of Fisheries under research project ENV9802 and by the Science–Industry Joint Project and Agreement of the Canadian Department of Fisheries and Oceans. We thank John Stevens for providing data on the Australian porbeagle catch, and Nancy Kohler and Peter Green for information on movements of tagged porbeagles.

References Aasen, O. (1961) Some Observations on the Biology of the Porbeagle Shark (Lamna nasus L.). ICES C.M. 1961: 109. International Council for the Exploration of the Sea, Copenhagen, Denmark, 7 pp. Aasen, O. (1963) Length and growth of the porbeagle (Lamna nasus, Bonnaterre) in the North West Atlantic. Fiskerdirektoratets Skrifter, Serie Havundersøkelser 13(6), 20–37.

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Ayers, D., Francis, M. P., Griggs, L. H. and Baird, S. J. (2004) Fish Bycatch in New Zealand Tuna Longline Fisheries, 2000–01 and 2001–02. New Zealand Fisheries Assessment Report No. 2004/46. Ministry of Fisheries, Wellington, New Zealand, 47 pp. Bigelow, H. B. and Schroeder, W. C. (1948) Sharks. In: Fishes of the Western North Atlantic. Part 1. Lancelets, Cyclostomes, Sharks (eds. A. E. Parr and Y. H. Olsen). Sears Foundation for Marine Research, New Haven, CT, pp. 59–546. Campana, S. E. and Joyce, W. N. (2004) Temperature and depth associations of porbeagle shark (Lamna nasus) in the Northwest Atlantic. Fisheries Oceanography 13, 52–64. Campana, S. E., Marks, L., Joyce, W., Hurley, P., Showell, M. and Kulka, D. (1999) An Analytical Assessment of the Porbeagle Shark (Lamna nasus) Population in the Northwest Atlantic. Document No. 99/158. Canadian Science Advisory Secretariat, Fisheries and Oceans, Ottawa, Ontario, Canada, 57 pp. Campana, S. E., Marks, L., Joyce, W. and Harley, S. (2001) Analytical Assessment of the Porbeagle Shark (Lamna nasus) Population in the Northwest Atlantic, with Estimates of Long-Term Sustainable Yield. Document No. 2001/067. Canadian Science Advisory Secretariat, Fisheries and Oceans, Ottawa, Ontario, Canada, 59 pp. Campana, S. E., Joyce, W., Marks, L., Natanson, L. J., Kohler, N. E., Jensen, C. F., Mello, J. J., Pratt, H. L. and Myklevoll, S. (2002a) Population dynamics of the porbeagle in the Northwest Atlantic Ocean. North American Journal of Fisheries Management 22, 106–121. Campana, S. E., Natanson, L. J. and Myklevoll, S. (2002b) Bomb dating and age determination of large pelagic sharks. Canadian Journal of Fisheries and Aquatic Sciences 59, 450–455. Campana, S. E., Joyce, W., Marks, L., Hurley, P., Natanson, L. J., Kohler, N. E., Jensen, C. F., Mello, J. J., Pratt Jr., H. L., Myklevoll, S. and Harley, S. (2008) The rise and fall (again) of the porbeagle shark population in the Northwest Atlantic. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Ellis, J. R. and Shackley, S. E. (1995) Notes on porbeagle sharks, Lamna nasus, from the Bristol Channel. Journal of Fish Biology 46, 368–370. Francis, M. P. and Duffy, C. (2005) Length at maturity in three pelagic sharks (Lamna nasus, Isurus oxyrinchus, and Prionace glauca) from New Zealand. Fishery Bulletin 103, 489–500. Francis, M. P. and Stevens, J. D. (2000) Reproduction, embryonic development and growth of the porbeagle shark, Lamna nasus, in the South-west Pacific Ocean. Fishery Bulletin 98, 41–63. Francis, M. P., Griggs, L. H. and Baird, S. J. (2001) Pelagic shark bycatch in the New Zealand tuna longline fishery. Marine and Freshwater Research 52, 165–178. Gauld, J. A. (1989) Records of Porbeagles Landed in Scotland, with Observations on the Biology, Distribution and Exploitation of the Species. Report No. 45. Fisheries Research Services, Aberdeen, Scotland, 15 pp. Jensen, C. F., Natanson, L. J., Pratt, H. L., Kohler, N. E. and Campana, S. E. (2002) The reproductive biology of the porbeagle shark, Lamna nasus, in the western North Atlantic Ocean. Fishery Bulletin 100, 727–738. Joyce, W., Campana, S. E., Natanson, L. J., Kohler, N. E., Pratt, H. L. and Jensen, C. F. (2002) Analysis of stomach contents of the porbeagle shark in the Northwest Atlantic Ocean. ICES Journal of Marine Science 59, 1263–1269. Kohler, N. E. and Turner, P. A. (2001) Shark tagging: A review of conventional methods and studies. Environmental Biology of Fishes 60, 191–223. Kohler, N. E., Casey, J. G. and Turner, P. A. (1995) Length–weight relationships for 13 species of sharks from the western North Atlantic. Fishery Bulletin 93, 412–418. Kohler, N. E., Casey, J. G. and Turner, P. A. (1998) NMFS Cooperative Shark Tagging Program, 1962–93: An atlas of shark tag and recapture data. Marine Fisheries Review 60(2), 1–87.

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Last, P. R. and Stevens, J. D. (1994) Sharks and Rays of Australia. CSIRO, Collingwood, Victoria, Australia. Mejuto, J. (1985) Associated Catches of Sharks, Prionace glauca, Isurus oxyrinchus, and Lamna nasus, with NW and N Spanish Swordfish Fishery, in 1984. ICES C.M. 1985: H42. International Council for the Exploration of the Sea, Copenhagen, Denmark, 16 pp. Mejuto, J. and Garcés, A. G. (1984) Shortfin Mako, Isurus oxyrinchus, and Porbeagle, Lamna nasus, Associated with Longline Swordfish Fishery in NW and N Spain. ICES C.M. 1984: G72. International Council for the Exploration of the Sea, Copenhagen, Denmark, 9 pp. Myklevoll, S. (1989) Norway’s Porbeagle Fishery. ICES C.M. 1989: H. International Council for the Exploration of the Sea, Copenhagen, Denmark, 16 pp. Natanson, L. J., Mello, J. J. and Campana, S. E. (2002) Validated age and growth of the porbeagle shark (Lamna nasus) in the western North Atlantic Ocean. Fishery Bulletin 100, 266–278. O’Boyle, R. N., Fowler, G. M., Hurley, P. C. F., Joyce, W. and Showell, M. A. (1998) Update on the Status of NAFO SA 3-6 Porbeagle Shark (Lamna nasus). Document No. 98/41. Canadian Science Advisory Secretariat, Fisheries and Oceans, Ottawa, Ontario, Canada, 58 pp. Stevens, J. D. (1976) First results of shark tagging in the North-east Atlantic, 1972–1975. Journal of the Marine Biological Association of the United Kingdom 56, 929–937. Stevens, J. D. (1990) Further results from a tagging study of pelagic sharks in the North-east Atlantic. Journal of the Marine Biological Association of the United Kingdom 70, 707–720. Stevens, J. D., Dunning, M. C. and Machida, S. (1983) Occurrences of the porbeagle shark, Lamna nasus, in the Tasman Sea. Japanese Journal of Ichthyology 30, 301–307. Svetlov, M. F. (1978) The porbeagle, Lamna nasus, in Antarctic waters. Journal of Ichthyology 18, 850–851. Templeman, W. (1963) Distribution of Sharks in the Canadian Atlantic (with Special Reference to Newfoundland Waters). Bulletin No. 140. Fisheries Research Board of Canada, Ottawa, Ontario, Canada, 77 pp. Yatsu, A. (1995) Zoogeography of the Epipelagic Fishes in the South Pacific Ocean and the Pacific Sector of the Subantarctic, with Special Reference to the Ecological Role of Slender Tuna, Allothunnus fallai. Bulletin No. 32. National Research Institute of Far Seas Fisheries, Shimizu, Japan, 145 pp.

Chapter 10

The Biology and Ecology of the Silky Shark, Carcharhinus falciformis Ramón Bonfil

Abstract The silky shark (Carcharhinus falciformis), an inhabitant of coastal and oceanic waters in tropical regions, is among the world’s most abundant and cosmopolitan shark species. It is caught in significant numbers in directed shark fisheries throughout its range and is an important bycatch in tropical tuna fisheries. On the basis of differences in life-history parameters, it is possible to identify at least three distinct populations inhabiting the Northwest Atlantic, the western-central Pacific, and the eastern Pacific. Data from the Indian Ocean are too sketchy to derive conclusions about a distinct population in this area. Silky sharks grow larger and mature at larger sizes in the Northwest Atlantic than in the western-central and eastern Pacific. Many populations mate and give birth during late spring and summer, but others do not have a well-defined reproductive season. Silky sharks are born after a 9- to 12-month gestation period and are thought to have 1 year of rest between pregnancies. Litter sizes range from 1 to 16 young, but are more commonly of 6–12 young. Estimates of age at maturity range from 4 to 10 years for males and from 7 to 12
years for females; maximum estimated age is 22
years. Given their importance for fishing communities worldwide and the increasing trend in shark catches, silky shark populations should be constantly monitored to assure their conservation and wise management. Key words: silky shark, Carcharhinus falciformis, Carcharhinidae, age and growth, distribution, fisheries, movements, reproduction, stock status.

Introduction The silky shark, Carcharhinus falciformis (Bibron, 1839), is a member of the requiem or gray sharks of the family Carcharhinidae and is one of the largest members of its genus, reaching up to 330 cm total length (TL). According to Garrick (1982), the species was originally described from the island of Cuba, but the adults and the juveniles were mistakenly classified as two separate species (with the adults attributed to C. floridanus) until both were synonymized by Garrick et al. (1964). Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Silky sharks get their common name from the distinctive smooth texture of their skin, which is covered with very fine and minute dermal denticles, making it softer to the touch than the considerably rougher skin of most other sharks. Apart from this peculiar skin texture, the silky shark can be recognized from similar members of Carcharhinus by (1) its falcate first dorsal and pectoral fins (thus its Latin name falciformis, meaning sickle shaped); (2) its relatively small first dorsal fin – whose origin is behind the free rear tips of the pectoral fins – with a rounded apex and a posterior margin slightly convex from the apex down, then slightly concave toward the posterior tip; (3) a very small and low second dorsal fin with a very long trailing tip that almost reaches the precaudal pit; and (4) the particular shape of its upper teeth. Young silky sharks have shorter pectoral fins and shorter heads than adults. The silky shark is one of the most frequently caught sharks in many tropical fisheries either as a target or as a bycatch species. But despite its commercial importance, our understanding of its biology and ecology is limited, and there is a genuine need for increased research, management, and perhaps even conservation work on silky sharks. This chapter presents a critical review of current knowledge about the biology, ecology, exploitation, and conservation of the silky shark.

Distribution, movements, and stock structure Geographic, depth, and age-related distribution The silky shark is one of the most common semipelagic sharks found in coastal and oceanic waters of all tropical oceans (Fig. 10.1). Its distribution seems to be limited to waters above 23ºC (Last and Stevens, 1994). Many of the apparent gaps in distribution in tropical seas may be due to limited records or misidentification with other species. Commercial fisheries throughout the world usually do not record catch by species, and silky sharks can be difficult to recognize from other members of Carcharhinus when one is not familiar with their identification. Silky sharks inhabit continental and insular shelves, slopes, and even offshore waters from the surface down to at least 500 m of depth, and have been occasionally recorded in water as shallow as 18 m (Compagno, 1984). They are more abundant along the edge of continental and insular shelves, although they can be found far offshore, especially adjacent to regions with deepwater reefs, in association with floating objects, and offshore island slopes. Strasburg (1958) noted that silky sharks were more abundant in the tropical Pacific as one approached the outer continental shelf, and Garrick (1982) pointed out that this species seems to have a wider latitudinal distribution along the continental margins than in open ocean or insular shelves. In the western Atlantic, and probably elsewhere, newborns have a more demersal lifestyle and, together with some of the early juveniles, occupy nursery grounds in shelf waters (Springer, 1967; Branstetter, 1987; Bonfil, 1997), while some juveniles and the subadults and adults occupy more oceanic habitats in slope waters (Bonfil, 1997). No strong evidence for sexual segregation in the silky shark has been reported, except by Strasburg (1958) for the Pacific Ocean populations.

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Fig. 10.1 Global distribution of silky sharks. The dark shading shows well-established distribution areas, while the light shading shows uncertain distribution (expected or possible presence, or records in need of confirmation).

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Movements and migrations Relatively little is known about the migrations and movements of the silky shark. Most of the available data come from the Northwest Atlantic, where more than 820 silky sharks have been tagged since 1963 under the National Marine Fisheries Service (NMFS) Cooperative Shark Tagging Program. The 54 recaptures to date (6.6% return rate) show that this species can migrate long distances quickly, with estimated maximum speeds of up to 60 km/day, ranking it fourth in speed after the blue shark (Prionace glauca, Carcharhinidae), the shortfin mako (Isurus oxyrinchus, Lamnidae), and the tiger shark (Galeocerdo cuvier, Carcharhinidae; Kohler et al., 1998). The majority of the sharks were tagged along the eastern coast of Florida and the northern Gulf of Mexico. The recaptures show that most silky sharks move northward along the East Coast, probably following the Gulf Stream, and only a few move southward into the Caribbean and even into the Gulf of Mexico (Fig. 10.2). At least one silky shark tagged off the Mexican coast had crossed the Gulf of Mexico from Yucatán to the northwestern coast of Florida (Bonfil, 1997). Silky sharks are commonly associated with schools of tuna and probably undertake long trips throughout their life, but this aspect of their ecology is poorly documented. The known maximum distance traveled by a silky shark is 1,339 km (Kohler et al., 1998). In the Pacific, silky sharks seem to move from the equator toward slightly higher latitudes during summer (Strasburg, 1958), and it is possible that this pattern of movement also occurs in other silky populations. In the Indian Ocean, adult silky sharks (including pregnant females) concentrate in the Gulf of Aden during the late spring and summer, but decrease in numbers during the rest of the year (Bonfil, 2003). Despite the fragmentary information, it is possible to reconstruct the patterns of distribution and movements of silky sharks in relation to age, based on the available literature (Strasburg, 1958; Springer, 1967; Branstetter, 1987; Bonfil et al., 1990, 1993; Bonfil, 1997) and personal observations of the author. In the Gulf of Mexico, silky sharks are born in the deeper parts of the continental shelf (such as the Campeche Bank). During the first few years of their life, neonates and young juveniles live in nursery grounds that appear to be associated with snapper reef areas. There, they lead a demersal/semipelagic lifestyle (they are known to be taken on both bottom and pelagic longlines), but soon move to a more offshore and pelagic existence. As they grow and approach about 130 cm TL, silky sharks switch to a more oceanic habitat, moving offshore and often joining schools of large pelagic fish such as tuna, probably traveling long distances with them. Adult silky sharks return seasonally to feed and reproduce in shelf waters, but they can also be found in oceanic areas. This general pattern of life-stage-related movement seems to be followed in other regions of the world (Cadena-Cárdenas, 2001) and is probably valid for the species as a whole. A more detailed understanding of the seasonal movements of silky sharks will require further studies using conventional and electronic tagging methodologies (i.e., archival and satellite tags).

Stock structure and genetic studies There is almost no information about the stock structure of silky sharks. Nevertheless, on the basis of variations in life-history parameters in different parts of the world, it appears

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n ⴝ 54

(a)

(b) Fig. 10.2 Maps showing tag and recapture locations of silky sharks tagged under the NMFS Cooperative Shark Tagging Program during 1962–1993. Arrowheads mark the recapture sites. (a) Map of movement in the Atlantic and Gulf of Mexico. (b) Close-up view of the US Atlantic and Gulf of Mexico. Source: Used with permission from Kohler et al. (1998).

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that there are several distinct populations (see Reproduction): One in the Northwest Atlantic Ocean, at least two in the Pacific Ocean (a western-central and an eastern population), and one in the Indian Ocean. Given the size of these ocean basins and the physical barriers between them, it is not surprising that genetic exchange between populations is restricted or even precluded. Whether there are more discrete populations within any of these oceans (e.g., western versus eastern Atlantic Ocean) and how much exchange and divergence there is between stocks are unknown, as no population genetic studies have been conducted for silky sharks. The chain of islands across the tropical Pacific may serve as a link for the apparently distinct eastern and western-central Pacific silky shark populations, but the population structure within the Pacific is as yet unknown. Conventional and electronic tagging programs implemented through observer programs onboard commercial fishing vessels, as well as genetic and biological studies, must be conducted for these questions to be answered.

Biology and ecology Reproduction The reproduction of the silky shark is probably the best known aspect of its biology. Except for studies on the morphology of the placentation (Gilbert and Schlernitzauer, 1965, 1966), only scattered observations of reproduction were made until the 1980s. More detailed studies in the Gulf of Mexico (Branstetter, 1987; Bonfil et al., 1993) and the Gulf of California (Cadena-Cárdenas, 2001) have improved our understanding of the reproductive cycle of this species. Silky sharks have one of the most evolved types of reproduction among the elasmobranchs: placental viviparity. In silky sharks, internal fertilization is followed by an approximately 12-month gestation period, after which up to 16 (more commonly 6–12) fully functional 65- to 80-cm-TL sharks are born. Maternal size is positively correlated to litter size (Cadena-Cárdenas, 2001), and miscellaneous observations suggest that the entire reproductive cycle spans 2 years, with a 1-year pregnancy followed by a “resting” year (Branstetter, 1987; Cadena-Cárdenas, 2001). Many silky shark populations do not show seasonality in the reproductive cycle (Strasburg, 1958; Bass et al., 1973; Cadenat and Blanche, 1981; Stevens, 1984a, b), but in some cases this could be an artifact of limited data (in time, space, or number of observations) rather than the existence of year-round reproduction. Branstetter (1987) and Bonfil et al. (1993) found a clear parturition and mating period from late spring to summer for Gulf of Mexico silky sharks. In other areas there is no obvious season for reproduction: Central Pacific populations have a parturition period spanning from February to August (S. Oshitani and H. Nakano, National Research Institute of Far Seas Fisheries, Japan, personal communication), and pregnant females from the eastern Atlantic (Cadenat and Blanche, 1981), the Gulf of Aden (Bonfil, 2003), and the Gulf of California (Cadena-Cárdenas, 2001) carry embryos of very different stages of development in the same month, indicating protracted mating/parturition. The role of environmental conditions in determining a well-defined reproductive season for this species in some regions warrants investigation.

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Table 10.1 Life-history parameters for silky sharks.a Region Northwest Atlantic Florida coast Northern Gulf of Mexico Campeche Bank Eastern Atlantic Unspecified Gulf of Guinea

Male TL maturity

Female TL maturity

TL at birth

Maximum TL

Reference

ca. 221 215–220 225

ca. 233 232 232–246

ca. 68–84 – 76

307 – 314

Springer (1960) Branstetter (1987)b Bonfil et al. (1993)

220

250

–

– 300

Cadenat and Blanche (1981) Bane (1966)b

–

238

–

Indian Southeastern Africa Aldabra Atoll Maldives

240 239 –

248–260 216 –

78–87 – 56–63

Western Pacific Northern Australia

210

215

–

Eastern Australia

214

202–208

–

Central Pacific

– –

213–218 –

66 65–81

236 245

Strasburg (1958) S. Oshitani and H. Nakano (personal communication)

Eastern Pacific

180

180

70

279

Cadena-Cárdenas (2001)

– – –

Bass et al. (1973)b Stevens (1984a)b Anderson and Ahmed (1993)

243

Stevens and McLoughlin (1991) (females)b Stevens (1984b)b

–

a

TL: total length in cm. Studies with fewer than 10 observations for size at maturity for either or both sexes, in which case the size given is usually the smallest mature specimen found. b

Reproductive parameters for silky sharks show relatively large geographic variability, but a clear analysis is obscured by the limited number of observations in some studies and to a lesser extent by the different methods used for the measurement of length (Table 10.1). Nevertheless, three groups, likely constituting distinct populations, are identifiable based on the consistency (coincidence of results between different studies for a given region) and robustness (number of sharks analyzed per study) of the data: A distinct group in the Northwest Atlantic, another in the west and central Pacific, and a third in the eastern Pacific. Northwestern Atlantic silky sharks reach sexual maturity and are born at considerably larger sizes (male sexual maturity at 215–225 cm TL, female sexual maturity at 232–246 cm TL, birth at 76 cm TL) than those in the western-central Pacific (male sexual maturity at 210–214 cm TL, female sexual maturity at 202–218 cm TL, birth at 66 cm TL). In contrast, eastern Pacific silky sharks show the smallest reported sizes at maturity (180 cm TL for both sexes). In addition, maximum sizes recorded for these areas follow the same trend (Table 10.1). Data from the eastern Atlantic are limited, but sizes at maturity appear to be within the range of those for the northwestern Atlantic. Available data from Indian Ocean silky sharks are conflicting, with a wide range of size at maturity for females, and males with larger sizes at maturity than females, probably due to the overall small number of specimens analyzed. However, except for the size at maturity for females reported by Stevens (1984a), it would appear that Indian Ocean silky sharks attain the

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Table 10.2 Von Bertalanffy growth model parameters for silky sharks.* Region

Sex

Northwestern Gulf of Mexico Southeastern Gulf of Mexico Central Pacific Central Pacific

Both Both Males Females

k

Linf (cm)

t0 (years)

Maximum age (years)

0.153 0.101 0.08 0.19

291 311 304.3 198.1

2.2 2.78 2.29 1.73

13
22
– –

*Linf is given in TL for the Gulf of Mexico, and in precaudal length for the central Pacific. Northwestern Gulf of Mexico data are from Branstetter (1987), southeastern Gulf data are from Bonfil et al. (1993), and central Pacific data are from S. Oshitani and H. Nakano (personal communication).

largest sizes at maturity. More precise estimates of size at maturity and birth are needed for the eastern Atlantic, Indian, and western-central Pacific Oceans.

Age and growth There are two published studies on the age and growth of silky sharks (Branstetter, 1987; Bonfil et al., 1993), plus one unpublished study (S. Oshitani and H. Nakano, personal communication). The first two are for populations in the northwestern and southeastern Gulf of Mexico, respectively, and the third study is for a central Pacific population. All used direct readings on thin sections of vertebral centra for age determination. Branstetter (1987) used unstained centra sections, whereas Bonfil et al. (1993) and Oshitani and Nakano (personal communication) used sections stained with alizarin-red-S. The two studies in the Gulf of Mexico found that silky sharks are born in late spring and summer, that growth is similar in both sexes, that a pair of growth bands is formed in the vertebrae every year (one translucent and one opaque), and that silky sharks are long-lived and have medium growth rates relative to other sharks, achieving sexual maturity at 6–10 years (males) and 7–12
years (females). Estimates of the von Bertalanffy growth model parameters derived by Branstetter (1987) and Bonfil et al. (1993) were slightly different (Table 10.2 and Fig. 10.3), but it is not known if this reflects true differences in growth or is due to differences in methodology or sample bias. Oshitani and Nakano found differences in growth between the sexes (Table 10.2), and estimated ages at first maturity of 4
years for males and 7–9 years for females. Their results are unique in finding significant growth differences between the sexes and fall outside the known pattern for most shark species in which females grow larger than males. It is possible that a lack of large females in their samples biased the growth model estimates toward a smaller asymptotic length for females, and also likely that an incomplete size range of male samples caused the model to overestimate the asymptotic length for males (Bonfil et al., 1993). Although none of these studies provided validation on the periodicity of ring formation, it appears from the verification methods used that the growth estimates are sufficiently accurate. However, to different extents the samples used for age determination in these studies did not include the full size structure of the population. Thus, at least some of the observed differences in growth parameters can be attributed to biases introduced by the size structure of the samples. Our knowledge of age and growth of silky sharks is still incomplete, especially considering that several populations of this species in other parts of the world remain unstudied.

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400

Total length (cm)

350 300 250 200

Southeastern Gulf of Mexico

150

Northwestern Gulf of Mexico

100

Pacific males

50

Pacific females

0 0

2

4

6

8

10

12

14

16

18

20

22

24

Age (years) Fig. 10.3 Von Bertalanffy growth curves for silky sharks from three different studies (Branstetter, 1987, for the northwestern Gulf of Mexico; Bonfil et al., 1993, for the southeastern Gulf of Mexico; and S. Oshitani and H. Nakano, personal communication, for the Pacific Ocean, after conversion of measurements in Table 10.2 from precaudal length to total length).

Diet Silky sharks are opportunistic feeders, feeding near the bottom as well as in the water column, and according to Springer (1979), adults are known to form large feeding aggregations when food is available. Compagno (1984) defines silky sharks as primarily piscivorous, a fact supported by the few detailed reports of stomach contents (Yoshimura and Kawasaki, 1985), but they also eat molluscs and crustaceans. No in-depth studies of their feeding habits exist, but the following list of prey is drawn from stomach analyses (Springer, 1979; Yoshimura and Kawasaki, 1985; Branstetter, 1987; Stevens and McLoughlin, 1991; Bonfil et al., 1993) – fish: sea catfish, yellowfin tuna, albacore, porcupine fish, monacanthids, balistids, groupers, snappers, ophichthid eels, Mugil spp., Katsuomus pelamis, Thunnus spp., Euthynnus spp., Scomber spp., Scomberomorus spp.; molluscs: squid, Octopus maya, Sepia spp., Argonauta spp.; crustaceans: pelagic crabs, Portunus spp., Kyphosus cinerascens, Myctophum spp., Elagatis bipinnulata, Decapterus macrosoma. Recent open-water video footage has provided probably the first direct record of silky shark feeding behavior in the wild. A group of silky sharks in the Pacific was filmed herding a shoal of clupeoid fishes, slowly scaring the fish into a more and more compact mass while driving them toward the surface. Once the shoal was sufficiently compact and practically trapped between the circling sharks and the air–water interface, the sharks proceeded to attack until not a single fish was left in the water.

Threats and status Silky sharks in tropical fisheries The preponderance of silky shark in fishery catches throughout tropical waters makes it a significant source of income for fishing communities around the world. Like other

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elasmobranchs, the silky shark is fished either directly or as bycatch. There are a few intense multispecies shark fisheries that catch large numbers of silky sharks, mainly in Mexico, Guatemala, El Salvador, Costa Rica, Sri Lanka, the Maldives, Yemen, and apparently Ivory Coast, and it may be a target species elsewhere as well (Anderson and Ahmed, 1993; Bonfil, 1994, 1997, 2003; Bonfil and Abdallah, 2004; R. Bonfil, unpublished data). It is probably caught in even greater quantities as bycatch in tropical tuna longline and purse-seine fisheries, especially when the gear is set near continental or insular shelves. Silky sharks are the most common shark bycatch of the eastern tropical Pacific (Kato, 1964; R. Bonfil, unpublished data) and the Gulf of Mexico (Russell, 1993) tuna fisheries, and are also frequently caught by tuna fleets in the Atlantic and Indian Oceans, as well as in tropical Australian waters (Cramer et al., 1997; Santana et al., 1997; Amorim et al., 1998; Marín et al., 1998; Stevens and Wayte, 1999). In many cases, most of the sharks are thrown overboard dead or alive, the fins being the only part that is utilized. There is a lack of accurate information about the actual quantity of silky sharks (and any other shark for that matter) being killed worldwide and within each region. However, given the size of the fishing operations in the Pacific Ocean, it is likely that the largest numbers of silky sharks are caught there. A rough estimate of the silky sharks taken as bycatch in tuna longline fisheries of the southern and central Pacific Ocean indicated that up to 900,000 individuals were caught during 1989 (Bonfil, 1994). Yet there is great uncertainty surrounding these calculations, and there are no estimates of numbers discarded alive and numbers actually killed, although given the common practice of finning among tuna fishermen it is likely that most sharks caught eventually die. Indeed, Clarke (2003) estimated that silky sharks are probably the second most important species (after blue sharks) supporting the Hong Kong fin trade. Furthermore, suspected misidentification between silky and blacktip (C. limbatus, Carcharhinidae) sharks in some Pacific tuna fisheries suggests that silky bycatch might be higher (S. Smith, NMFS, personal communication; C. Lennert, Inter-American Tropical Tuna Commission (IATTC), personal communication). Inadequate data obscure the quantity of silky sharks that are landed by the various shark-fishing fleets of the world. FAO catches of silky sharks in Sri Lankan fisheries for the period 1960–1998 averaged 11,000 metric tons (t)/year and oscillated around 20,000 t/year over the last 6 years. However, according to Bonfil (1994), only about 75% of these catches are actually attributable to silky sharks; Sri Lankan scientists report (information courtesy of the Fishery Information Data and Statistics Unit, FAO) that only about 13,000 t/year of silky sharks were landed in the mid-1990s. In the Gulf of Mexico, silky sharks are regularly caught as part of Mexican multispecies shark fisheries, and to a lesser extent in US shark and tuna/swordfish fisheries, but in most cases the catch is not recorded at the species level. Recently instituted observer programs have partially alleviated this problem, at least in the Gulf of Mexico (Cramer et al., 1997; Gonzalez-Ania et al., 1997). Landings of silky shark by US commercial fisheries off the East Coast were estimated at 14.5 and 6.5 t (dressed weight) for 2000 and 2001, respectively (Cortés and Neer, 2002).

Stock assessment and fisheries management There have been only a few attempts to conduct stock assessment of silky sharks because of limited landings data and the absence of estimates of population sizes or indices of

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abundance for most populations. Bonfil (1990) detected growth overfishing of silky sharks in the Yucatán fishery by applying Beverton and Holt’s yield per recruit analysis. Subsequent research using a simulation model of the population dynamics of silky sharks in this fishery indicated that banning the catch of juveniles was the best alternative for management of this stock, considering fishery conditions in the late 1980s (Bonfil, 1996). For the Pacific Ocean, Oshitani and Nakano (personal communication) characterized the silky shark stock as stable. Their study, using generalized linear model–standardized catchper-unit-effort (CPUE) data and separable virtual population analysis, estimated a total catch of 13,000–20,000 t against a biomass of 170,000–240,000 t, with a resulting fishing mortality level of F  0.061–0.096 and a stable CPUE trend for 1992–1998, which was higher than that found in 1967–1970. In the Gulf of Mexico, Baum and Myers (2004) compared the catch rates of silky sharks from tuna surveys in the 1950s against catch rates from the commercial pelagic longline fishery in the 1990s (targeting tunas, swordfish, and sharks) and found a drop of nearly 91% in silky shark abundance. While the exact magnitude of this decline is subject to debate owing to differences in the mode of fishing between the two data sets, there is little doubt that silky shark populations have undergone significant declines in the Gulf of Mexico over the last 40 years of fishing. Given their life-history characteristics, silky sharks have a moderate capacity to recover from overexploitation. Smith et al. (1998, 2008), in a quantitative analysis of the intrinsic rebound potential for 26 different shark species, listed the silky shark in the middle of the range (intrinsic rebound potential of 0.043, within a range of 0.017–0.136). Similar results, confirming the moderate capacity of silky sharks for population growth, were obtained through additional demographic modeling (Cortés, 2002, 2008; Beerkircher et al., 2003).

Conservation of silky sharks During preparation of the 2000 IUCN Red List of Endangered Species, the silky shark was assessed as a Lower Risk, Least Concern species (thus it does not appear on the Red List). This classification was based on the lack of evidence for strong declines in abundance, the generally high abundance of the silky shark where it occurs, and its wide distribution in all tropical oceans; these last two characteristics make it likely to be one of the five most abundant shark species in the world. Populations of the northern Indian Ocean, tropical Pacific Ocean, and Northwest Atlantic Ocean were classified as Data Deficient because of the lack of information on the number of sharks dying in relation to the abundance of the species (it is known that silky sharks are exploited in these areas, but there are no statistics of these catches nor indices of abundance for the stocks). In light of the findings outlined earlier, it is likely that this species will be assigned threatened status, at least for the Northwest Atlantic population, in the next publication of the Red List. Several international fishery organizations have recently initiated specific actions to lower shark bycatch in pelagic (tuna and billfish) fisheries. The IATTC is determining the extent of shark identification problems in the eastern tropical Pacific tuna purse-seine fishery (C. Lennert, personal communication). The International Commission for the Conservation of Atlantic Tunas (ICCAT) has enhanced its data recording system to include detailed shark bycatch by species since 1996, which resulted in a stock assessment for shortfin mako and

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blue sharks in the Atlantic (Babcock and Nakano, 2008). Unfortunately, lack of adequate data precludes a similar assessment for silky sharks in the immediate future. With renewed commitment and effort, stock assessment and management of the fisheries that affect silky and other sharks can be dramatically improved within a few years. However, comprehensive plans for shark management in international waters, perhaps through suitable agreements among fishery organizations, are also needed to establish informed and sustainable management of the world’s diverse shark populations.

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and the Status of the Fisheries (eds. H. L. Pratt Jr., S. H. Gruber and T. Taniuchi). NOAA Technical Report NMFS 90. NOAA/NMFS, Silver Spring, MD, pp. 427–441. Bonfil, R., Mena, R. and de Anda, D. (1993) Biological parameters of commercially exploited silky sharks, Carcharhinus falciformis, from the Campeche Bank, México. In: Conservation Biology of Elasmobranchs (ed. S. Branstetter). NOAA Technical Report NMFS 115. NOAA/NMFS, Silver Spring, MD, pp. 73–86. Branstetter, S. (1987) Age, growth and reproductive biology of the silky shark, Carcharhinus falciformis, and the scalloped hammerhead, Sphyrna lewini, from the northwestern Gulf of Mexico. Environmental Biology of Fishes 19, 161–173. Cadena-Cárdenas, L. (2001) Biología reproductiva Carcharhinus falciformis (Chondrichthyes: Carcharhiniformes: Carcharhinidae), en el Golfo de California. Bachelor’s thesis, Departamento de Biología Marina, Universidad Autónoma de Baja California Sur, La Paz, Mexico, 66 pp. Cadenat, J. and Blanche, J. (1981) Requins de Mediterranee et d’Atlantique. Faune tropicale XXI. ORSTOM, Paris, France, 330 pp. (as cited in Branstetter, 1987). Clarke, S. C. (2003) Quantification of the Trade in Shark Fins. Ph.D. thesis, Imperial College London, London, UK, 327 pp. Compagno, L. J. V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Parts 1 and 2. FAO Fisheries Synopsis No. 125. FAO, Rome, Italy, 655 pp. Cortés, E. (2002) Incorporating uncertainty into demographic modeling: Application to shark populations and their conservation. Conservation Biology 16, 1048–1062. Cortés, E. (2008) Comparative life history and demography of pelagic sharks. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Cortés, E. and Neer, J. A. (2002) Updated Catches of Sharks. Shark Bowl Working Document SB/02/15. NOAA Fisheries, Panama City, FL, 62 pp. Cramer, J., Bertolino, A. and Scott, G. P. (1997) Estimates of recent shark bycatch by US vessels fishing for Atlantic tuna and tuna-like fishes. ICCAT Collective Volume of Scientific Papers 48(3), 117–128. Garrick, J. A. F. (1982) Sharks of the Genus Carcharhinus. NOAA Technical Report NMFS 445. NOAA/NMFS, Silver Spring, MD, 194 pp. Garrick, J. A. F., Backus, R. H. and Gibbs Jr., R. H. (1964) Carcharhinus floridanus, the silky shark, a synonym of C. falciformis. Copeia 1964, 369–375. Gilbert, P. W. and Schlernitzauer, D. A. (1965) Placentation in the silky shark, Carcharhinus falciformis and bonnetshark, Sphyrna tiburo. The Anatomical Record 151(3), 452. Gilbert, P. W. and Schlernitzauer, D. A. (1966) The placenta and gravid uterus of Carcharhinus falciformis. Copeia 1966, 451–457. Gonzalez-Ania, L. V., Ulloa-Ramírez, P. A., Lee, D. W., Brown, C. J. and Brown, C. A. (1997) Description of Gulf of Mexico longline fisheries based upon observer programs from Mexico and the United States. ICCAT Collective Volume of Scientific Papers 48(3), 308–316. Kato, S. (1964) Sharks of the Genus Carcharhinus Associated with the Tuna Fishery in the Eastern Tropical Pacific Ocean. Circular 172. US Fish and Wildlife Service, Bureau of Commercial Fisheries, Washington, DC, 22 pp. Kohler, N. E., Casey, J. G. and Turner, P. A. (1998) NMFS Cooperative Shark Tagging Program, 1962–93: An atlas of shark tag and recapture data. Marine Fisheries Review 60(2), 1–87. Last, P. R. and Stevens, J. D. (1994) Sharks and Rays of Australia. CSIRO, Collingwood, Victoria, Australia. Marín, Y. H., Brum, F., Barea, L. C. and Chocca, J. F. (1998) Incidental catch associated with swordfish longline fisheries in the south-west Atlantic Ocean. Marine and Freshwater Research 49, 633–639.

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Russell, S. J. (1993) Shark bycatch in the northern Gulf of Mexico tuna longline fishery, 1988–91, with observations on the nearshore directed shark fishery. In: Conservation Biology of Elasmobranchs (ed. S. Branstetter). NOAA Technical Report NMFS 115. NOAA/NMFS, Silver Spring, MD, pp. 19–29. Santana, J. C., Delgado de Molina, A., Delgado de Molina, R., Ariz, J., Stretta, J. M. and Domalain, G. (1997) Lista faunística de las especies asociadas a las capturas de atún de las flotas de cerco comunitarias que faenan en las zonas tropicales de los océanos Atlántico e Indico. ICCAT Collective Volume of Scientific Papers 48(3), 129–137. Smith, S. E., Au, D. W. and Show, C. (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678. Smith, S. E., Au, D. W. and Show, C. (2008) Intrinsic rates of increase in pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Springer, S. (1960) Natural history of the sandbar shark, Eulamia milberti. Fishery Bulletin 61, 38. Springer, S. (1967) Social organization of shark populations. In: Sharks, Skates and Rays (eds. P. W. Gilbert, R. F. Mathews and D. P. Ralls). Johns Hopkins University Press, Baltimore, MD, pp. 141–174. Springer, S. (1979) Report on Shark Fishing in the Western Central Atlantic. United Nations Development Programme/FAO, Panamá. Stevens, J. D. (1984a) Life-history and ecology of sharks at Aldabra Atoll, Indian Ocean. Proceedings of the Royal Society of London Series B 222, 79–106. Stevens, J. D. (1984b) Biological observations on sharks caught by sport fishermen off New South Wales. Australian Journal of Marine and Freshwater Research 35, 573–590. Stevens, J. D. and McLoughlin, K. J. (1991) Distribution, size and sex composition, reproductive biology and diet of sharks from northern Australia. Australian Journal of Marine and Freshwater Research 42, 151–199. Stevens, J. D. and Wayte, S. E. (1999) A Review of Australia’s Pelagic Shark Resources. Final Report Project 98/107. Fisheries Research and Development Corporation, Deakin West, Australian Capital Territory, Australia, 64 pp. Strasburg, D. W. (1958) Distribution, abundance, and habits of pelagic sharks in the central Pacific Ocean. Fishery Bulletin 58, 335–361. Yoshimura, H. and Kawasaki, S. (1985) Silky shark (Carcharhinus falciformis) in the tropical water of Western Pacific. Report of the Japanese Group for Elasmobranch Studies 20, 6–10.

Chapter 11

The Biology and Ecology of the Oceanic Whitetip Shark, Carcharhinus longimanus Ramón Bonfil, Shelley Clarke and Hideki Nakano

Abstract The oceanic whitetip shark (Carcharhinus longimanus) is a common circumtropical predator and is taken as bycatch in many oceanic fisheries. This summary of its life history, distribution and abundance, and fishery-related information is supplemented with unpublished data taken during Japanese tuna research operations in the Pacific Ocean. Oceanic whitetips are moderately slow-growing sharks that do not appear to have differential growth rates by sex, and individuals in the Atlantic and Pacific Oceans seem to grow at similar rates. They reach sexual maturity at approximately 170–200 cm total length (TL), or 4–7 years of age, and have a 9- to 12-month embryonic development period. Pupping and nursery areas are thought to exist in the central Pacific, between 0ºN and 15ºN. According to two demographic metrics, the resilience of C. longimanus to fishery exploitation is similar to that of blue and shortfin mako sharks. Nevertheless, reported oceanic whitetip shark catches in several major longline fisheries represent only a small fraction of total shark catches, and studies in the Northwest Atlantic and Gulf of Mexico suggest that this species has suffered significant declines in abundance. Stock assessment has been severely hampered by the lack of species-specific catch data in most fisheries, but recent implementation of species-based reporting by the International Commission for the Conservation of Atlantic Tunas (ICCAT) and some of its member countries will provide better data for quantitative assessment. On the basis of its life-history characteristics, this species is presently considered by the World Conservation Union to be vulnerable to, but not currently threatened by, pelagic fisheries. Key words: oceanic whitetip shark, Carcharhinus longimanus, Carcharhinidae, age and growth, reproduction, distribution, abundance, fisheries.

Introduction The oceanic whitetip shark (Carcharhinus longimanus, Carcharhinidae) is one of the most common top predators in open waters of all tropical oceans of the world, and is the only truly oceanic shark of its genus. This species and the blue shark (Prionace glauca, Carcharhinidae) are the most abundant oceanic sharks, and they seem to have evolved an Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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efficient partitioning of the oceanic environment, with blue sharks dominating the temperate seas and oceanic whitetips prevailing in tropical areas (Nakano, 1996; Matsunaga and Nakano, 1999). Despite its worldwide distribution and frequent appearance in most high-seas fishery catches in tropical areas, little attention has been paid to oceanic whitetip shark biology and ecology. Since Bigelow and Schroeder (1948) pointed out that “astonishingly little is known of the habits of longimanus, considering that it is one of the members of its genus that has been recognized the longest,” only a handful of papers have focused on this shark. Studies by Backus et al. (1956) in the western North Atlantic and Strasburg (1958) in the eastern Pacific Ocean were among the first to describe the distribution, abundance, size structure, diet, behavior, sex segregation, and reproduction of the oceanic whitetip. However, nearly 30 years passed before Saika and Yoshimura (1985) further reported on the natural history of this species, and theirs was a limited analysis of the ecology and biology of populations in the western Pacific Ocean. More recently, a paper by Savel’ev and Chernikov (1994) assessed the presumed ability of oceanic whitetip sharks to search for food from smells in the air, and Seki et al. (1998) and Lessa et al. (1999) studied the age, growth, and reproduction of populations in the Pacific Ocean and equatorial West Atlantic, respectively. The latest contributions to our knowledge of this species come from a pair of papers, Baum et al. (2003) and Baum and Myers (2004), describing declines in shark populations in the Northwest Atlantic and Gulf of Mexico. We also present data from fisheries that catch oceanic whitetip sharks, as well as unpublished data on the bycatch from Japanese tuna research and training cruises (including a total of 209,530 longline sets and 444 million hooks).

Distribution and movements The oceanic whitetip shark is a tropical, epipelagic species occurring from the surface to at least 152 m depth. It has a clear preference for open ocean waters and its abundance increases away from continental and insular shelves (Backus et al., 1956; Strasburg, 1958; Compagno, 1984). Although it can be found in waters between 15ºC and 28ºC, it is most commonly found in waters with temperatures above 20ºC. It is one of the most abundant oceanic sharks, and although it generally does not school, it can form aggregations around food sources. Catch rates for this species have been shown to decrease with increasing depth between 80 and 280 m, suggesting that oceanic whitetips are found in shallow surface waters more commonly than other pelagic sharks, such as the bigeye thresher (Alopias superciliosus, Alopiidae; Nakano et al., 1997). Preliminary data from Japanese research and training tuna longliners (H. Nakano, unpublished data) indicate that, in the Pacific Ocean, oceanic whitetips are most abundant in a belt between 10ºN and 10ºS, are common between 20ºN and 20ºS, and can occur up to about 30ºN in the northwestern Pacific (Fig. 11.1). These data also show that pregnant oceanic whitetips occur mainly in a wide area of the North Pacific between 140ºW and 150ºE, with higher concentrations in the central part of this distribution just above 10ºN (Fig. 11.2). Newborn sharks occur between the equator and 20ºN, but mainly in a narrow strip just above 10ºN in the central Pacific, coincident with the higher concentrations of

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100 40
N

10 1

20
N

0


20
S

40
S 120
E

140
E

160
E

180


160
W 140
W 120
W

100
W

80
W

Fig. 11.1 Catch rate of oceanic whitetip sharks by Japanese tuna research and training vessels for each sampled 1° quadrant in the Pacific Ocean. Bubble size is proportional to the number of sharks per thousand hooks (aggregated data from 209,530 longline sets with a total of 444 million hooks for the period 1992–1998, from the National Research Institute of Far Seas Fisheries).

40
N 30
N 20
N 10
N 0
10
S 20
S

Pregnant females Newborns

30
S 120
E

140
E

160
E

180


160
W

140
W

120
W

100
W

Fig. 11.2 Distribution of pregnant females and newborns of oceanic whitetip shark in the tropical Pacific Ocean (data from Japanese tuna research and training vessels for the period 1992–1998, from the National Research Institute of Far Seas Fisheries).

pregnant females. This suggests that the area between 150ºW and 180ºW and just above 10ºN might be a pupping ground for oceanic whitetip sharks. However, incomplete sampling limits a better definition of this area. Little is known of the migrations and movements of this species; Backus et al. (1956) reported that oceanic whitetip sharks move out of the Gulf of Mexico during the winter

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and may move southward from the waters north of Cape Hatteras when temperatures drop. They hypothesize that the avoidance of shallow-water habitats may be a mechanism to avoid competition for food with faster-swimming coastal sharks. In the Cooperative Shark Tagging Program of the US National Marine Fisheries Service, 542 oceanic whitetips were tagged in the Atlantic Ocean between 1962 and 1993, but only 6 were recaptured. Maximum time at liberty was 3.3 years, maximum distance traveled was 2,270 km, and maximum estimated speed was 32 km/day (Kohler et al., 1998). These data indicate movements from the northeastern Gulf of Mexico to the Atlantic Coast of Florida, from the Mid-Atlantic Bight to southern Cuba, from the Lesser Antilles west into the central Caribbean Sea, from east to west along the equatorial Atlantic, and from off southern Brazil in a northeasterly direction.

Biology and ecology Diet Oceanic whitetip sharks are one of the main apex predators in tropical open waters, and feed mostly on oceanic teleosts and cephalopods (Backus et al., 1956). Their diet consists of lancetfish, oarfish, threadfins, barracuda, jacks, dolphinfish, tuna, skipjack and other scombrids, white marlin, and squid, and occasionally stingrays, seabirds, turtles, marine gastropods, crustaceans, carrion from marine mammals, and garbage (Compagno, 1984).

Reproduction Similar to other carcharhinid species, the oceanic whitetip shark is viviparous with placental embryonic development. There are few reproductive studies for this species, and most of the information comes from the Pacific Ocean populations considered in Seki et al. (1998). In the North Pacific, mating takes place during June and July, and parturition occurs from February to July. These findings, based on a sample size of 52 embryos, suggest a 9- to 12-month embryonic development period. From a more limited sample size for the South Pacific (n  16), parturition appears to occur in November. Size at maturity ranged from 168 to 196 cm total length (TL) for males and from 175 to 189 cm TL for females, although a 137-cm-TL pregnant female was also recorded but not fully investigated (lengths converted from precaudal (PL) to total length using Seki et al.’s formula of TL1.397  PL). Size at birth was between 55 and 75 cm TL, and the number of embryos in a litter ranged from 1 to 14, with a mode of 5 and an average of 6.2 (Seki et al., 1998). There was a weak positive correlation between female size and litter size. Ancillary observations (Bigelow and Schroeder, 1948; Backus et al., 1956; Bass et al., 1973; Lessa et al., 1999) on the reproduction of oceanic whitetip sharks in other areas of the world have usually been based on smaller sample sizes than in Seki et al. (1998). In South African waters, males were found to attain sexual maturity around 194 cm TL and females around 170–180 cm TL; in the northwestern Atlantic, females mature between 189 and 198 cm TL; both sexes attain maturity between 180 and 190 cm TL in the equatorial western Atlantic. Size at birth is around 65–75 cm TL in the northwestern Atlantic and

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60–65 cm TL off South Africa. A positive correlation between female size and number of pups per litter was found in the northwestern Atlantic, where litter size averages 6. In this area, the gestation period is about 12 months, and mating and parturition have a defined period from late spring to summer. In South African waters, parturition also occurs in late spring and summer. There may be a pupping ground in the equatorial western Atlantic off Brazil.

Age and growth Until recently, little was known of the age and growth of this species. The first studies were conducted by Saika and Yoshimura (1985), who provided initial estimates for the growth coefficient (k) of 0.04–0.09 for both sexes in the western Pacific based on vertebrae of 13 specimens (Table 11.1). Also working in the Pacific, Seki et al. (1998) subsequently analyzed thin sections of vertebral centra from 111 males and 114 females and estimated a higher k of 0.103. No difference in growth between the sexes was observed. The authors assumed that one growth band is laid per year, and estimated through marginal increment analysis that annuli formation takes place in spring. According to their results, both sexes mature at 4–5 years of age, and the maximum age in their sample was 11 years. In the western equatorial Atlantic, Lessa et al. (1999) analyzed unstained thin sections of vertebral centra from 110 individuals (44 male, 60 female, and 6 of undetermined sex) and also found no evidence of differential growth between the sexes. Growth coefficients varied from 0.075 for back-calculated lengths to 0.099 using the observed-length-at-age method (Table 11.1). However, the authors reported that back-calculated lengths did not match well with those from direct readings, thus raising some doubts about their backcalculated growth model parameters. This study assumed that one translucent ring and one opaque ring were deposited each year and estimated that annuli are completely formed by July. The age at sexual maturity for both sexes using the observed-length-atage method was estimated at 6–7 years. The maximum age found in the female samples was 13 years, although using their von Bertalanffy growth equation they estimated a maximum age of 17 years for a larger female that was not aged through vertebral analysis. Prior to the age and growth studies by Seki et al. (1998) and Lessa et al. (1999), Branstetter (1990) used growth parameters to classify a number of carcharhinoid and lamnoid sharks by life-history strategy. Using the earlier estimates of k from Saika and Yoshimura (1985), and an estimate of the asymptotic average maximum body size (L) Table 11.1 Von Bertalanffy growth parameters for oceanic whitetip sharks. Reference

Bass et al. (1973) Saika and Yoshimura (1985) Seki et al. (1998) Lessa et al. (1999) Observed length-at-age Back-calculated

Growth coefficient, k

Asymptotic body size, L

Hypothetical age at length zero, t0

– 0.04–0.09 0.103

270–300 TL – 244.58 PL

– – 2.698

0.099 0.075

284.9 TL 325.4 TL

3.391 3.342

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from Bass et al. (1973) (Table 11.1), the oceanic whitetip shark was characterized as a slow-growing species on the basis of k less than 0.10, growth in the first year less than 30% of birth length, and length at birth greater than 20% of maximum length. Other pelagic sharks, such as the blue shark (k  0.11–0.25), shortfin mako (Isurus oxyrinchus, Lamnidae; k  0.20–0.27), and silky shark (Carcharhinus falciformis, Carcharhinidae; k  0.10–0.15), were classified as fast-growing species (Branstetter, 1990). The more recent estimates of the growth coefficient for the oceanic whitetip by Seki et al. (1998) and Lessa et al. (1999) suggested that its growth characteristics are intermediate to the archetypal slow- and fast-growth species described by Branstetter (1990).

Demographic analyses Demographic techniques have been used to characterize the vulnerability of various species to exploitation based on survival, maturation, and fecundity estimates. Although demographic metrics are sensitive to various assumptions and input parameters, such studies provide a framework for relative comparison of oceanic whitetips to other pelagic and coastal shark species. Using a method that incorporates density dependence, Smith et al. (1998) compared the productivities of 26 sharks representing five orders and nine families. In this method, the maximum sustainable yield (MSY) population size is approximated by assuming that total mortality is equal to double the adult instantaneous natural mortality (M ) for each species. Two different assumptions are applied regarding species-specific fecundity (b), resulting in two different values of r2M (the intrinsic rate of increase when total mortality is 2M, or the intrinsic rebound potential) for each shark. In this study, the oceanic whitetip was ranked as the sixth most productive shark of the 26 species considered, with a midpoint for the two r2M estimates that was higher than that for the blue shark but slightly lower than that for the common thresher (Alopias vulpinus; Table 11.2). Cortés (2002) also used demographic analysis, and an assumption that vital rates are independent of density over time, to estimate values of the population growth rate (λ, where r  log λ) for 38 species of sharks representing four orders and nine families. In this study, the value of λ for the oceanic whitetip from the western Pacific was eleventh highest among 41 shark populations (Table 11.2). This value indicates that oceanic whitetip productivity is in the range of other pelagic sharks, including Prionace glauca and Alopias vulpinus.

Table 11.2 Demographic metrics for three common pelagic sharks: The intrinsic rate of increase and the population growth rate provide relative measures of species resilience to exploitation. Common name

Scientific name

Common thresher Oceanic whitetip Blue

Alopias vulpinus Carcharhinus longimanus Prionace glauca

Intrinsic rate of increase, r2M (midpoint of 1.00b and 1.25b estimates) (Smith et al., 1998) 0.084 0.081 0.074

Population growth rate, λ (Cortés, 2002)

1.125 1.117 1.401

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Fisheries Catch and catch-rate data Although oceanic whitetip sharks are seldom explicitly targeted, they are one of the most common bycatch species in tuna fisheries in offshore tropical waters. They are frequently caught in small-scale multispecies shark fisheries, for example, in the Gulf of Aden (R. Bonfil, unpublished data) and along the Pacific coast of Central America (Bonfil and Abdallah, 2004). Despite their abundance, quantification of catch numbers or biomass for this species is hindered by the lack of complete and accurate logbook data. Using an estimate of hooks deployed north of 20ºN in the Pacific by Japanese and South Korean longline fleets in 1988, and hooking rates of 0.07 oceanic whitetips per 1,000 hooks from Strasburg (1958), Bonfil (1994) estimated that 7,253 oceanic whitetips, or about 145 metric tons (t), were taken annually as incidental catch in the North Pacific. Applying Strasburg’s (1958) hooking rate for the eastern equatorial Pacific of 5.46 whitetips per 1,000 hooks, and an estimate of total hooks fished by Japanese, South Korean, Taiwanese, and Australian longliners in that area in 1989, Bonfil (1994) estimated that another 539,946 individuals (about 10,799 t) were taken annually in the central and South Pacific. Similar extrapolations were not provided for the Atlantic and Indian Oceans owing to high expected variation in catch rates by area and season. Other fishery-specific studies provide anecdotal information on catches and catch rates for oceanic whitetips in the Atlantic, Indian, and Pacific Oceans. In Brazilian waters, Lessa et al. (1999) found they were the second most abundant shark species caught by longline in equatorial regions between 1992 and 1997. In contrast, observer data collected from the Japanese longline fleet in the Atlantic in the period 1995–2003 indicated that oceanic whitetips composed less than 1% of all shark bycatch (Senba and Nakano, 2004). Such differences in catch rates are likely due to potential differences in fishing gear and mode of operation between the two fleets, and notably the localized activity of Brazilian longliners compared to the wider coverage of the Japanese fleet. Very low catches of oceanic whitetip sharks relative to other sharks were also found in the US Atlantic pelagic longline fishery logbooks, where the average number of individuals taken per year between 1990 and 2000 was 165, compared to an average annual take of 17,380 blue sharks and 11,953 shortfin makos (Cortés, 2001). Data from Spanish surface longline fisheries for 1999 indicated that of the 32.7 t of sharks landed from the Atlantic that year, only 0.2 t (0.6%) were oceanic whitetips (Mejuto et al., 2001). They were present in 4.72% of the sets of French and Spanish purse-seine tuna fleets in the tropical eastern Atlantic (Santana et al., 1997). Using available data from the longline fleets based in Uruguay and Brazil, Domingo (2004) reported that this species appears to be rather rare (only 0.006 sharks per 1,000 hooks) in the southern Atlantic; data from the Uruguayan fleet in fishing grounds off western equatorial Africa showed a catch rate of 0.09 sharks per 1,000 hooks. In the Indian Ocean, data from research longline vessels in the late 1960s showed that C. longimanus composed 3.4% of the shark catch, compared to 22.5% in the western Pacific and 21.3% in the eastern Pacific (Taniuchi, 1990). Oceanic whitetips were present in 16% of the tuna purse-seine sets of Spanish and French fleets in the western Indian

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Ocean (Santana et al., 1997). Recent surveys in the Red Sea and Gulf of Aden have shown this species to be a common catch in medium- and small-scale directed multispecies shark fisheries using gill nets (Bonfil, 2003). Analyses of data from Japanese research longliners in the Pacific offer a historical comparison between the late 1960s and the early 1990s for the pelagic environment stretching from Papua New Guinea to Hawaii (Matsunaga and Nakano, 1999; Nakano, 1999). Oceanic whitetip catch per unit effort (CPUE) was characterized for 1967–1970 (n  912 sets; 1,777,000 hooks) and 1992–1995 (n  5,700 sets; 12,293,000 hooks) and standardized for differences in hook depth as fishing operations changed through the years. Significant changes in CPUE between the two periods were only observed in the eastern half of the study area (east of 180º latitude). Immediately north of the equator (0–10ºN), C. longimanus CPUE increased by 40–80%, whereas farther north (10–20ºN) catch rates decreased by 30–50%. The authors concluded that further standardization would be necessary to more clearly interpret abundance trends. Two studies analyzing catch-rate indices for oceanic whitetips in the Northwest Atlantic and Gulf of Mexico suggested a strong trend of declining populations. In the Northwest Atlantic, US commercial pelagic longline catch rates for C. longimanus from 1992 to 2000 showed declines of 70%, although the authors caution that such trends are more difficult to interpret for oceanic shark species because their habitats extend beyond the fishing grounds (Baum et al., 2003). In the Gulf of Mexico, research longline surveys in 1954 and 1957 (n  170 sets; 82,972 hooks) were used to establish baseline catch rates that were then compared to observer data from US commercial longlines between 1995 and 1999 (n  275 sets; 219,461 hooks; Baum and Myers, 2004). In the earlier period, the oceanic whitetip was the most common shark caught, accounting for 61% of all hooked sharks and present in 64% of all sets. By the latter period, however, catch rates for this species had declined by 99%. Despite differences in gear and operational deployment between the two surveys, the authors concluded that this species is in danger of extirpation at this particular edge of its distribution.

Utilization Numerous products are derived from oceanic whitetip sharks: meat and skin for human consumption, hides for leather production, and vitamin A derived from liver oil (Compagno, 1984; McCoy and Ishihara, 1999; Vannuccini, 1999). Fins from this species are one of the most distinctive and common products in the Asian shark fin trade and compose at least 2% by weight of shark fins auctioned in Hong Kong (Clarke et al., 2005, 2006). Molecular genetic testing of 23 fin samples collected from nine traders and representing three ocean basins demonstrated a 100% concordance between the trade name “Liu Qiu” (Chinese for “rolling ball,” presumably a reference to the fin’s rounded edges) and C. longimanus (Clarke et al., 2006). Shark fin consolidators, working outside of Asia, reportedly include oceanic whitetip fins within the category of “brown” sharks (McCoy and Ishihara, 1999), which indicates that some oceanic whitetip fins may be sold in unspecified mixed lots. As a result, quantities labeled as “Liu Qiu” in the shark fin market may underestimate the true quantity of oceanic whitetip fins in trade. Despite the availability of “Liu Qiu” or “brown” fins in the market, these fins are not graded

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particularly highly by shark fin traders (Parry-Jones, 1996; McCoy and Ishihara, 1999; Fong and Anderson, 2000). Wholesale prices for oceanic whitetip fin sets (size and weight not given) originating in the South Pacific ranged from US $45 to $85 for the period 1997–2003 (Clarke, 2004). Because of economic and operational differences, the utilization of this species varies from fleet to fleet. The Mexican tuna fleet in the Gulf of Mexico retains 95% of oceanic whitetip sharks caught as bycatch for local consumption or sale, whereas the US fleet in the same area keeps only 7% of individuals, and releases 69% alive (Gonzalez-Ania et al., 1997). Taiwanese longliners reportedly retain about half of the oceanic whitetip carcasses in their bycatch, whereas Japanese longliners are believed to discard all of the meat from this species (McCoy and Ishihara, 1999). Studies of oceanic whitetips landed by the coastal fisheries off Japan indicate that the proportion of retained carcass meat to whole weight for this species varies from 53% to 60% (Matsunaga et al., 2003).

Management and conservation In 1996, ICCAT began requesting that parties submit their shark data using a form that lists eight species of pelagic sharks, including oceanic whitetip shark (Kebe et al., 2001). However, ICCAT recognized that most of its member countries would have difficulties in immediately fulfilling this obligation, and this has proven to be the case. In the 2001 posting of the ICCAT shark database (ICCAT, 2001), only five countries – Brazil, Mexico, Spain, St. Lucia, and the United States – had reported oceanic whitetip catches (Table 11.3). More recently, national reports presenting observer data for the French purse-seine fishery off West Africa (Goujon, 2003) and the Japanese longline fleet in the North and South Atlantic (Senba and Nakano, 2004) have included data for the oceanic whitetip, indicating that other fisheries do collect species-specific catch data for this shark. Since 1997, Japan has required the recording of oceanic whitetip sharks in a separate category in the logbooks of all fisheries. No stock assessments have been conducted for C. longimanus, in large part because of the lack of historical catch and abundance indices. As more fisheries, such as those reporting to ICCAT, begin recording pelagic shark catches by species, the prospects for rigorously assessing the impact on oceanic whitetip stocks will improve. Evaluation of the conservation status of this species is hampered by the limited availability of standardized catch and abundance data, and the resulting absence of stock assessment studies. Oceanic whitetips are considered a highly migratory species under Annex I Table 11.3 Catches of oceanic whitetip sharks reported to ICCAT’s shark database (ICCAT, 2001). Country Brazil Spain Mexico St. Lucia United States Total

Years 1992–1993 1997–1998 1994–1995 1995 1983–1999

Total number of sharks

Total weight of sharks (round weight, t)

201 – 57 – 2,022

– 13.466 5.480 0.076 62.680

2,280

81.702

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of the 1982 Convention on the Law of the Sea (FAO, 1994). Castro et al. (1999) classified this species as vulnerable to overfishing on the basis of its slow growth, limited reproductive potential, and high rate of bycatch in pelagic fisheries. The World Conservation Union’s (IUCN) Red List considers the oceanic whitetip shark to be a Lower Risk/Near Threatened species (IUCN, 2004). A better understanding of oceanic whitetip biological parameters and improved fishery statistics are needed to identify management and conservation measures. Until such data are available, precautionary management measures are warranted.

Acknowledgments R. Bonfil and S. Clarke thank the Japan Society for the Promotion of Science for the postdoctoral fellowships that supported them in the preparation of this manuscript. All authors acknowledge the assistance of the Ecologically Related Species Team of the National Research Institute of Far Seas Fisheries.

References Backus, R. H., Springer, S. and Arnold, E. L. J. (1956) A contribution to the natural history of the white-tip shark, Pterolamiops longimanus (Poey). Deep Sea Research 3, 178–188. Bass, A. J., D’Aubrey, J. S. and Kistnasamy, N. (1973) Sharks of the East Coast of Southern Africa. I. The Genus Carcharhinus (Carcharhinidae). Report No. 33. Oceanographic Research Institute, Durban, South Africa. Baum, J. K. and Myers, R. A. (2004) Shifting baselines and the decline of pelagic sharks in the Gulf of Mexico. Ecology Letters 7, 135–145. Baum, J. K., Myers, R. A., Kehler, D. G., Worm, B., Harley, S. J. and Doherty, P. A. (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299, 389–392. Bigelow, H. B. and Schroeder, W. C. (1948) Fishes of the Western North Atlantic. Part 1. Lancelets, Cyclostomes, Sharks (eds. A. E. Parr and Y. H. Olsen). Sears Foundation for Marine Research, New Haven, CT, 576 pp. Bonfil, R. (1994) Overview of World Elasmobranch Fisheries. FAO Fisheries Technical Paper No. 341. FAO, Rome, Italy, 119 pp. Bonfil, R. (2003) Consultancy on Elasmobranch Identification and Stock Assessment in the Red Sea and Gulf of Aden. Final report to the Regional Organization for the Conservation of the Environment of the Red Sea and Gulf of Aden, Jeddah. Wildlife Conservation Society, New York, 195 pp. Bonfil, R. and Abdallah, M. (2004) Field Identification Guide to the Sharks and Rays of the Red Sea and Gulf of Aden. FAO Species Identification Guide for Fishery Purposes. FAO, Rome, Italy, 71 pp. Branstetter, S. (1990) Early life-history implications of selected carcharhinoid and lamnoid sharks of the Northwest Atlantic. In: Elasmobranchs As Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries (eds. H. L. Pratt Jr., S. H. Gruber and T. Taniuchi). NOAA Technical Report NMFS 90. NOAA/NMFS, Silver Spring, MD, pp. 17–28. Castro, J. I., Woodley, C. M. and Brudek, R. L. (1999) A Preliminary Evaluation of Status of Shark Species. FAO Fisheries Technical Paper No. 380. FAO, Rome, Italy.

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Clarke, S. (2004) Trade in Shark Products in Malaysia, Singapore and Thailand. Southeast Asian Fisheries Development Center, Bangkok, Thailand, 53 pp. Clarke, S. C., McAllister, M. K. and Michielsens, C. G. J. (2005) Estimates of shark species composition and numbers associated with the shark fin trade based on Hong Kong auction data. Journal of Northwest Atlantic Fishery Science 35, 453–465. Clarke, S., Magnusson, J. E., Abercrombie, D. L., McAllister, M. and Shivji, M. S. (2006) Identification of shark species composition and proportion in the Hong Kong shark fin market based on molecular genetics and trade records. Conservation Biology 20, 201–211. Compagno, L. J. V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Parts 1 and 2. FAO Fisheries Synopsis No. 125. FAO, Rome, Italy, 655 pp. Cortés, E. (2001) Catches and catch rates of pelagic sharks from the northwestern Atlantic, Gulf of Mexico, and Caribbean. ICCAT Collective Volume of Scientific Papers 54(4), 1164–1181. Cortés, E. (2002) Incorporating uncertainty into demographic modelling: Application to shark populations and their conservation. Conservation Biology 16, 1048–1062. Domingo, A. (2004) ¿Adónde fue el longimanus? ELASMOVISOR, Boletim Informativo da SBEEL, Fundação Universidade Federal do Rio Grande, Rio Grande, Brazil. FAO (Food and Agriculture Organization) (1994) World Review of Highly Migratory Species and Straddling Stocks. FAO Fisheries Technical Paper No. 337. FAO, Rome, Italy. Fong, Q. S. W. and Anderson, J. L. (2000) Assessment of the Hong Kong shark fin trade. INFOFISH International 1, 28–32. Gonzalez-Ania, L. V., Ulloa-Ramírez, P. A., Lee, D. W., Brown, C. J. and Brown, C. A. (1997) Description of Gulf of Mexico longline fisheries based upon observer programs from Mexico and the United States. ICCAT Collective Volume of Scientific Papers 48(3), 308–316. Goujon, M. (2003) Informations sur les captures accessoires des thoniers senneurs gérés par les armements français d’après les observations faites par les observaterurs embarqués pendant les plan de protection des thonidés de l’Atlantique de 1997 à 2002. ICCAT Collective Volume of Scientific Papers 56(2), 414–431. ICCAT (International Commission for the Conservation of Atlantic Tunas) (2001) Database of all Atlantic shark catch statistics currently available (updated 25 June 2001). www.iccat.es. IUCN (World Conservation Union) (2004) IUCN Shark Specialist Group Red List assessments, 2000–2003 (updated March 2004). www.flmnh.ufl.edu/fish/organizations/ssg/summary2004.pdf. Kebe, P., Restrepo, V., Palma, C. and Cheatle, J. (2001) An overview of shark data collection by ICCAT. ICCAT Collective Volume of Scientific Papers 54(4), 1107–1122. Kohler, N., Casey, J. G. and Turner, P. A. (1998) NMFS Cooperative Shark Tagging Program, 1962–93: An atlas of shark tag and recapture data. Marine Fisheries Review 60, 1–87. Lessa, R., Santana, F. M. and Paglerani, R. (1999) Age, growth and stock structure of the oceanic whitetip shark, Carcharhinus longimanus, from the southwestern equatorial Atlantic. Fisheries Research 42, 21–30. Matsunaga, H. and Nakano, H. (1999) Species composition and CPUE of pelagic sharks caught by Japanese longline research and training vessels in the Pacific Ocean. Fisheries Science 65, 16–22. Matsunaga, H., Nakano, H., Ishibashi, Y. and Nakayama, K. (2003) Estimation of the amount of shark landing by species in the main fishing ports of Japan. Nippon Suisan Gakkaishi 69, 178–184 (in Japanese). McCoy, M. A. and Ishihara, H. (1999) The Socio-economic Importance of Sharks in the US Flag Areas of the Western and Central Pacific. Administrative Report 274, AR-SWR-99-01. Southwest Fisheries Science Center, NMFS, Long Beach, CA.

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Mejuto, J., Garcia-Cortes, B. and de la Serna, J. M. (2001) Preliminary scientific estimations of by-catches landed by the Spanish surface longline fleet in 1999 in the Atlantic Ocean and Mediterranean Sea. ICCAT Collective Volume of Scientific Papers 54(4), 1150–1163. Nakano, H. (1996) Distribution of pelagic elasmobranchs in the North Pacific Ocean. Kaiyo Monthly 28(7), 407–415 (in Japanese). Nakano, H. (1999) Elasmobranch conservation movements and pelagic shark stocks. Kaiyo Monthly 16, 102–111. Nakano, H., Okazaki, M. and Okamoto, H. (1997) Analysis of catch depth by species for tuna longline fishery based on catch by branch lines. Bulletin of the National Research Institute of Far Seas Fisheries 34, 43–62. Parry-Jones, R. (1996) TRAFFIC report on shark fisheries and trade in Hong Kong. In: The World Trade in Sharks: A Compendium of TRAFFIC’s Regional Studies. TRAFFIC International, Cambridge, UK, pp. 83–143. Saika, S. and Yoshimura, H. (1985) Oceanic whitetip shark (Carcharhinus longimanus) in the Western Pacific. Report of the Japanese Group for Elasmobranch Studies 20, 11–21 (in Japanese; available at jses.ac.affrc.go.jp/report/20/20-3.pdf). Santana, J. C., Delgado de Molina, A., Delgado de Molina, R., Ariz, J., Stretta, J. M. and Domalain, G. (1997) Lista faunística de las especies asociadas a las capturas de atún de las flotas de cerco comunitarias que faenan en las zonas tropicales de los océanos Atlántico e Indico. ICCAT Collective Volume of Scientific Papers 48(3), 129–137. Savel’ev, S. V. and Chernikov, V. P. (1994) Oceanic whitetip shark Carcharhinus longimanus can use aerial olfaction for food searching. Voprosy Ikhtiologii 34(2), 219–225 (in Russian). Seki, T., Taniuchi, T., Nakano, H. and Shimizu, M. (1998) Age, growth and reproduction of the oceanic whitetip shark from the Pacific Ocean. Fisheries Science 64, 14–20. Senba, Y. and Nakano, H. (2004) Summary of Species Composition and Nominal CPUE of Pelagic Sharks Based on Observer Data from the Japanese Longline Fishery in the Atlantic Ocean from 1995 to 2003. ICCAT Standing Committee on Research and Statistics Report No. 2004/117. ICCAT, Madrid, Spain. Smith, S. E., Au, D. W. and Show, C. (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678. Strasburg, D. W. (1958) Distribution, abundance, and habits of pelagic sharks in the central Pacific Ocean. Fishery Bulletin 58, 335–361. Taniuchi, T. (1990) The role of elasmobranchs in Japanese fisheries. In: Elasmobranchs As Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries. NOAA Technical Report NMFS 90. NOAA/NMFS, Silver Spring, MD, pp. 415–426. Vannuccini, S. (1999) Shark Utilization, Marketing and Trade. FAO Fisheries Technical Paper No. 389. FAO, Rome, Italy, 470 pp.

Chapter 12

The Biology and Ecology of the Blue Shark, Prionace glauca Hideki Nakano and John D. Stevens

Abstract The blue shark (Prionace glauca) is widely distributed in the world’s oceans. For an elasmobranch, it is relatively productive, giving birth to an average of 30 pups after a 9- to 12-month gestation. Annual fecundity is uncertain, but individual females may breed every year. The young are usually born in spring and summer, and the pupping and nursery areas seem to be located in transition zones where there is a large prey biomass for the juveniles. Growth is relatively rapid, with males maturing at 4–6 years and females at 5–7 years. The blue shark diet consists mainly of small pelagic fish and cephalopods, particularly squid. Relative abundance is generally lowest in equatorial waters and increases with latitude. Distinct sex and size segregation is evident, with size generally decreasing with increasing latitude. Blue sharks are highly migratory, with complex movement patterns related to reproduction and to the distribution of prey. Tagging studies have shown extensive movements with numerous transoceanic migrations; distance moved increases with age. Blue sharks are a major bycatch of longline and gill-net fleets, but because of poor reporting, the magnitude of the catch and mortality is not reflected by official statistics, and the limited population assessments carried out to date do not indicate major impacts on their populations. A number of blue shark populations are thought to be stable despite heavy fishing pressure. Key words: blue shark, Prionace glauca, Carcharhinidae, reproduction, age and growth, migration, movement models, fishery catch, population assessment.

Introduction The blue shark (Prionace glauca, Carcharhinidae) is an oceanic species found worldwide in temperate and tropical waters. It is a distinctive shark with a slender body and long pectoral fins, and with indigo blue dorsal coloration, metallic blue flanks, and abruptly white undersides. The blue shark is a relatively large species, reaching 383 cm in length, with males growing to a similar size as females. It is the most abundant pelagic shark, and large numbers are caught by the world’s fisheries, principally as bycatch on longlines and in gill nets. Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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This shark is a major component of the international shark fin trade (Clarke, 2003). Of all the pelagic sharks, it is the best studied, with most published information relating to the Atlantic and North Pacific populations. Nakano and Seki (2003) provided an extensive summary of blue shark biological data. Its widespread distribution, high initial abundance, and moderate productivity have given the blue shark the reputation of being resilient to fishing pressure. However, there is a need for a more coordinated ocean-basin approach to population assessments for this species.

Biology and ecology Age and growth Age and growth have been relatively well studied in the North Pacific and North and South Atlantic blue shark populations. About 50% of male blue sharks in the western Atlantic are sexually mature by 218 cm total length (TL), although some may reach maturity as small as 182 cm. Females are subadult from 173 to 221 cm TL and fully mature from 221 cm (Pratt, 1979). In the Gulf of Guinea, in the eastern Atlantic, 50% of females were pregnant at 217 cm (Castro and Mejuto, 1995). In the North Pacific, maturity for both sexes is about 200 cm TL (Suda, 1953; Nakano et al., 1985). Pregnant sharks as small as 183 cm have been recorded from the northeastern Pacific (Williams, 1977). In the South Pacific, males mature at about 229–235 cm and females at 205–229 cm (Francis and Duffy, 2005). Blue shark aging studies have generally used vertebral rings, which appear to be relatively easy to read. Manning and Francis (2005) fitted a range of alternative growth models to blue shark length-at-age data and preferred a Schnute model. They found that females appear to approach a lower mean asymptotic maximum length and grow at a faster rate than males, contrary to aging studies using data from other oceans. However, they suggest that this may be due to sampling bias. Published von Bertalanffy growth parameters are presented in Table 12.1. Generally, these studies indicate a longevity of about 20 years, with males maturing at 4–6 years and females at 5–7 years. Validation of age estimates for blue sharks is still needed.

Reproduction The reproductive mode in blue sharks is placental viviparity. Gestation lasts 9–12 months, and litters average about 30 pups (up to 135 have been recorded); birth size is usually 35–50 cm TL (Suda, 1953; Gubanov and Grigor’yev, 1975; Pratt, 1979; Stevens, 1984; Stevens and McLoughlin, 1991; Nakano, 1994; Castro and Mejuto, 1995; Snelson et al., 2008). Reproduction has been reported as seasonal in most areas, with the young often born in spring or summer (Pratt, 1979; Stevens, 1984; Nakano et al., 1985; Nakano, 1994), although the periods of ovulation and parturition may be extended (Strasburg, 1958; Hazin et al., 1994). It is unclear whether adult females breed each year, and so annual fecundity is unknown. In the North Atlantic, Pratt (1979) recognized three groups of females – immatures, subadults, and matures – and suggested the following reproductive cycle. Four- and five-year-old females (173–221 cm TL) arrive on the continental shelf off southern

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Table 12.1 Von Bertalanffy growth parameters for the blue shark, Prionace glauca, in the North Pacific and North and South Atlantic Oceans.* Source Pacific Ocean Cailliet et al. (1983) Tanaka (1984) Nakano (1994) Manning and Francis (2005) Atlantic Ocean Aasen (1966) Stevens (1975) Aires-da-Silva (1996) Henderson et al. (2001) Skomal and Natanson (2003) Lessa et al. (2004)

Sex

L⬁

K

t0

n

Length measurement

Male Female Male Female Male Female Male Female

295.3 241.9 308.2 256.1 289.7 243.3 342.9 267.5

0.175 0.251 0.094 0.116 0.129 0.144 0.088 0.126

⫺1.113 ⫺0.795 ⫺0.993 ⫺1.306 ⫺0.756 ⫺0.849 ⫺1.257 ⫺1.047

38 88 n.a. n.a. 148 123 140 288

TL

Combined Combined Combined Combined Male Female Combined

394.0 423.0 340.0 376.5 282.3 310.8 352.0

0.133 0.110 0.138 0.120 0.180 0.130 0.160

⫺0.801 ⫺1.035 ⫺1.075 ⫺1.330 ⫺1.350 ⫺1.770 ⫺1.010

n.a. 82 308 30 287 119 236

TL TL TL TL FL

PCL PCL FL

TL

*n.a.: not available; TL: total length; FL: fork length; PCL: precaudal length.

New England in late May and early June. Mating occurs with males of 215 cm (6 years) and larger; the skin of females is about three times thicker than that of males to withstand the courtship bites of males. Four-year-old females actively mate but are too undeveloped to store sperm in their nidamental glands. Five-year-old females mate and store sperm; the following spring these 6-year-old sharks stay offshore and fertilize their eggs in May or June. Embryos take 9–12 months to develop and are born from April to July. Gravid females have ripe ovarian eggs, suggesting that another fertilization is imminent. In the South Atlantic off southeastern Brazil, mating occurs from December to February (Amorim, 1992). Similar-sized females (165–225 cm fork length) are found 3 months later off northeastern Brazil, where they ovulate and are fertilized mainly from March to May (Hazin, 1993; Hazin et al., 1994). In the Gulf of Guinea, Castro and Mejuto (1995) found similar-sized females from June to August that were mostly pregnant with 10- to 30-cm embryos; these authors found that embryo size increased to the east. Newborn young were never found off northeastern Brazil or in the Gulf of Guinea, and were very unusual off southeastern Brazil. Parturition appears to occur outside these areas, possibly off South Africa (F. Hazin, Universidade Federal Rural de Pernambuco, Recife, Brazil, personal communication). Gubanov and Grigor’yev (1975) described a situation in the equatorial Indian Ocean off eastern Africa that suggests ovulation and fertilization occur at a similar time and area as in the southwestern equatorial Atlantic (F. Hazin, personal communication).

Diet The diet of blue sharks consists mainly of small pelagic fish and cephalopods, particularly squid; invertebrates (mostly pelagic crustaceans), small sharks, cetaceans (possibly as carrion), and seabirds are also taken (Compagno, 1984; Clarke et al., 1996; Henderson et al.,

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2001). While most of the fish prey is pelagic, bottom fishes also feature in the diet. Blue sharks are known to feed throughout the 24-hour period but have been reported to be more active at night, with highest activity in the early evening (Sciarrotta and Nelson, 1977). In the Northwest Atlantic, blue sharks make frequent vertical excursions between the surface and several hundred meters depth. Carey and Scharold (1990) thought this behavior was a hunting tactic in response to prey distribution, as well as being related to behavioral thermoregulation. In eastern Australian waters, data from pop-off archival transponding tags show vertical excursions to at least 600 m depth, presumably related to feeding (J. D. Stevens, unpublished data).

Distribution and movements Distribution The blue shark is one of the most wide-ranging of all sharks, being found throughout tropical and temperate seas from about 60ºN to 50ºS latitude. It is oceanic and epipelagic, and ranges from the surface to at least 600 m depth; occasionally it occurs close inshore where the continental shelf is narrow. The blue shark prefers temperatures of 12–20ºC and is found at greater depths in tropical waters (Last and Stevens, 1994). Relative abundance is generally lowest in equatorial waters and increases with latitude (Strasburg, 1958; Sivasubramaniam, 1963; Nakano, 1994; Stevens and Wayte, 1999). Distinct size and sex segregation is usually evident. For example, off the east coast of Australia, body size decreases, and the proportion of females increases, with increasing southerly latitude (Stevens and Wayte, 1999; West et al., 2004). Catches tend to increase with distance from land (Strasburg, 1958; Gubanov and Grigor’yev, 1975; Hazin et al., 1990).

Migration and movements Blue sharks are highly migratory with complex movement patterns related to reproduction and the distribution of prey. A seasonal shift in population abundance to higher latitudes is associated with oceanic convergence or boundary zones, as these are areas of higher productivity. Tagging studies of blue sharks have demonstrated extensive movements in the Atlantic with numerous trans-Atlantic migrations (Kohler and Turner, 2008), which are probably accomplished by swimming slowly and utilizing the major current systems (Stevens, 1976, 1990; Casey, 1985). More limited tagging in the Pacific has also shown extensive movements of up to 9,200 km (P. Saul, National Institute of Water and Atmospheric Research, Wellington, New Zealand, personal communication). Nakano (1994) suggested the following movement model for the North Pacific. Mating takes place in early summer at 20–30ºN, and pregnant females migrate north to the parturition grounds by the next summer (Fig. 12.1(a)). Birth occurs in early summer in pupping grounds that are located at 35–45ºN. Two- to five-year-old females (135–200 cm TL) occur in the pupping grounds and the region just to the north, including the Gulf of Alaska. Twoto four-year-old males (135–200 cm TL) occupy the pupping grounds and the area just to the

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140⬚E

160⬚E

180⬚

160⬚W

Nursery ground

140⬚W

Subadult

Parturition ground

40⬚N

Mating ground 20⬚N Pregnant female

Adult

0⬚

Female (a) 140⬚E

40⬚N

160⬚E

180⬚

160⬚W

140⬚W

Parturition ground Nursery ground

Subadult

Mating ground 20⬚N Adult

0⬚

Male (b) Fig. 12.1 Blue shark migration models for the North Pacific for (a) females and (b) males (Nakano, 1994).

south (Fig. 12.1(b)). The pupping and nursery areas are located in the sub-Arctic boundary, where there is a large prey biomass for the juveniles, who remain there for 5–6 years prior to maturity (Nakano and Nagasawa, 1996). Adults occur mainly from equatorial waters to the south of the nursery grounds.

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Stevens (1990) expanded the movement model of Casey (1985) for blue sharks in the North Atlantic. Much of this model is based on tagging data; while these data are extensive, it should be noted that the release sites are mostly in coastal areas and may impart some bias on the interpretation of movements. In the western Atlantic, where the population consists mainly of juveniles of both sexes, subadult females, and adult males, sharks move offshore into the Gulf Stream or south along the margins of the Gulf Stream during late summer, autumn, and winter, some traveling as far south as the Caribbean and South America (Fig. 12.2(a)). Juvenile and subadult females, most of which have recently mated, move offshore and probably do not return; some of these sharks probably ride the current systems to the eastern Atlantic. During spring, sharks move inshore from the Gulf Stream and north along the continental shelf; during summer they occur in large numbers off southern New England, Georges Bank, Nova Scotia, and the Grand Banks (Casey, 1985) (Fig. 12.2(b)). Mature females are rare in inshore waters of the western North Atlantic. In the eastern Atlantic during winter, adult females are found in the area of the Canary Islands and African coast at about 27–32ºN (Muñoz-Chápuli, 1984), at which time many are pregnant (Casey, 1985) (Fig. 12.2(a)). Adult males are found farther north off the Portuguese coast, along with juvenile and subadult females that have moved south from northern Europe; some mating of subadult females probably occurs at this time. Immature males are not caught in this region and may be offshore. In spring and summer, adult males and females are found around 32–35ºN, where they mate (Fig. 12.2(b)). Immature males also occur in this area. Adult females seem to have a seasonal reproductive cycle, while males and subadult females are sexually active throughout the year (Pratt, 1979; Stevens, 1984). The immature females migrate north to northern Europe, where they are common in summer, especially off the coast of southwestern England (Stevens, 1976). Birth probably occurs in early spring; nursery areas are found in the Mediterranean and off the Iberian peninsula, particularly off Portugal and near the Azores (Aires-da-Silva et al., 2008), but extend as far north as the Bay of Biscay. Juvenile sharks remain in the nursery areas and do not take part in the extensive migrations of the adults until they reach a length of about 130 cm (Stevens, 1976; Muñoz-Chápuli, 1984). In the eastern Atlantic, mature females, pregnant sharks, and newborn young are common during certain seasons, and it seems that a large proportion of the North Atlantic breeding population occurs in this region (Casey, 1985).

Threats and status Fisheries Blue sharks are rarely a targeted commercial species, but they are a major bycatch of longline and gill-net fisheries, particularly from nations with high-seas fleets. Because there is usually no requirement for these fisheries to record their blue shark catch, the magnitude of the catch is not reflected in catch statistics. Blue sharks are the most common pelagic shark taken by sportfishermen, particularly in the United States, Europe, and Australia (Babcock, 2008). While blue shark catch data from longline and gill-net fishing are sparse,

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80⬚W

70

60

50

40

30

20

10

0

50⬚N

Mainly juvenile females

and Mainly juvenile s ale subadult fem

Adult males and juvenile and subadult females

Adult females – many pregnant

Ma inl y ad juve ult ni ma le a les nd

40

30

20

10

0 (a) 70

60

50

40

30

20

inl y fem juve ale nile s

80⬚W

0

50⬚N Nursery

Ma

Some mating?

10

d

Pupping

an ile en les v u y j ma inl ult Ma ad

40

Mating

30

20

10

0 (b) Fig. 12.2 Blue shark migration models for the North Atlantic for (a) autumn–winter and (b) spring–summer.

it is clear that very large quantities are being taken globally. The high-seas blue shark catch from North Pacific fisheries in 1988 was estimated at 5 million individuals, or 100,000 metric tons (t), at an average weight of 20 kg per shark (Nakano and Watanabe, 1992), and the catch from longline fleets in the Pacific in 1994 was about 137,000 t (Stevens, 2000).

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Bonfil (1994) estimated that 6.2–6.5 million blue sharks were taken annually by high-seas fisheries around the world. Although these figures are only rough estimates, they give some idea of the magnitude of the exploitation.

Population status Stock structure and population sizes of the blue shark are not known, but tagging data suggest that blue sharks in the North Atlantic may be a single stock (Kohler and Turner, 2008). Atlantic stocks in the Northern and Southern Hemispheres are likely separate because of the opposite reproductive seasons, although tag returns indicate some movement between the North and South Atlantic (Kohler et al., 1998). Limited tag data from the Pacific also indicate exchange between the Indian and South Atlantic Oceans (J. D. Stevens, unpublished data). Although blue sharks are among the most widespread, fecund, and faster-growing elasmobranchs, their general life-history characteristics may nonetheless limit their ability to withstand heavy fishing pressure. Taniuchi (1990) reported no significant decline in catch per unit effort (CPUE) of Japanese research and training vessels in the tropical Indian and Pacific Oceans during the period 1973–1985. Nakano and Watanabe (1992) assessed the impact of high-seas fisheries on North Pacific stocks, and after estimating catches and using forward-projecting cohort simulations, they believed that the catch rates of the late 1980s did not cause significant population decline. However, Wetherall and Seki (1992) stated that some of the assumptions in their model could not be supported by available information. Matsunaga and Nakano (1999) examined Japanese longline species composition and CPUE data from two time periods (1967–1970 and 1992–1995) and two areas (0–10ºN and 10–20ºN) in the Pacific and concluded that there had been no significant change in blue shark abundance. Nakano (1996), using standardized Japanese longline CPUE data from 1971 to 1993, found no significant trend with time in blue shark catch rates in the Atlantic or Indian Oceans, but noted a 20% decrease in the North Pacific. A deterministic age-structured model was used by Nakano et al. (1999) to examine the effects of high-seas fishing on blue sharks in the North Pacific, and they concluded that past and current fishing pressure has had little impact on the stocks. By contrast, Simpfendorfer et al. (2002) and Hueter and Simpfendorfer (2008) used research longline CPUE data for the Northwest Atlantic and showed an 80% decline for males between the mid-1980s and the early 1990s, but no significant decline in female CPUE. Baum et al. (2003) also showed a decline of about 60% in CPUE data for the Northwest Atlantic, based on commercial logbook data. Clarke (2003) suggested that blue sharks are being exploited at rates that are close to, or possibly exceeding, maximum sustainable yield. Recent assessments by the International Commission for the Conservation of Atlantic Tunas (ICCAT) indicated that blue sharks appear to be well above the biomass that would sustain maximum sustainable yield in both the North and South Atlantic (Babcock and Nakano, 2008). West et al. (2004) provided a review of blue shark assessments, including trophic and ecosystem models, and carried out a yield analysis that suggests the maximum sustainable harvest in weight is likely to be only a few percent of the unexploited stock biomass, implying low harvest rates. Although a comprehensive stock assessment of blue sharks is still lacking, no evidence currently exists to suggest that their

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stock status is in a critical state. However, the growing evidence of declines challenges the view that blue sharks are immune to overfishing (Hueter and Simpfendorfer, 2008). The blue shark is one of the most ubiquitous chondrichthyans and the best studied of the pelagic sharks, particularly in the Atlantic and Pacific Oceans. It is captured in huge numbers by a wide range of fisheries, mainly as bycatch, and features prominently in the international shark fin trade. The limited number of population assessments carried out to date are conflicting with regard to the status of this shark (probably owing to poor data quality), and a coordinated ocean-basin approach is needed to improve the data collection, analysis, and assessment for this species.

Acknowledgments Thanks to Grant West (CSIRO Marine and Atmospheric Research) for producing Fig. 12.1. We also thank Dr. Shelley Clarke for her suggestions and help on the final draft.

References Aasen, O. (1966) Blahaien, Prionace glauca (Linnaeus), 1758. Fisken og Havet 1, 1–15. Aires-da-Silva, A. A. (1996) Contribution to the Knowledge of the Age and Growth of the Blue Shark, Prionace glauca (Carcharhinidae), in the North Atlantic. Undergraduate thesis, Universidade do Algarve, Faro, Portugal, 73 pp. Aires-da-Silva, A., Ferreira, R. L. and Pereira, J. G. (2008) Case study: Blue shark catch rate patterns from the Portuguese swordfish longline fishery in the Azores. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Amorim, A. F. (1992) Estudo da biologia, pesca e reproducao do cacao azul, Prionace glauca L. 1758, capturado no sudeste e sul do Brasil. Ph.D. thesis, Universidade Estadual Paulista, Rio Claro, São Paulo, Brazil, 176 pp. Babcock, E. A. (2008) Recreational fishing for pelagic sharks worldwide. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Babcock, E. A. and Nakano, H. (2008) Data collection, research, and assessment efforts for pelagic sharks by the International Commission for the Conservation of Atlantic Tunas. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Baum, J. K., Myers, R. A., Kehler, D. G., Worm, B., Harley, S. J. and Doherty, P. A. (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299(5605), 389. Bonfil, R. (1994) Overview of World Elasmobranch Fisheries. FAO Fisheries Technical Paper No. 341. FAO, Rome, Italy, 119 pp. Cailliet, G. M., Martin, L. K., Harvey, J. T., Kusher, D. and Welden, B. A. (1983) Preliminary studies on the age and growth of blue, Prionace glauca, common thresher, Alopias vulpinus, and shortfin mako, Isurus oxyrinchus, sharks from California waters. In: Proceedings of the International Workshop on Age Determination of Oceanic Pelagic Fishes: Tunas, Billfishes, and Sharks (eds. E. D. Prince and L. M. Pulos). NOAA Technical Report NMFS 8. NOAA/NMFS, Silver Spring, MD, pp. 179–199.

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Carey, F. G. and Scharold, J. V. (1990) Movements of blue sharks (Prionace glauca) in depth and course. Marine Biology 106, 329–342. Casey, J. G. (1985) Transatlantic migrations of the blue shark: A case history of cooperative shark tagging. In: Proceedings of the First World Angling Conference, Cap d’Agde, France, 12–18 September 1984 (ed. R. H. Stroud). International Game Fish Association, Dania Beach, FL, pp. 253–267. Castro, J. A. and Mejuto, J. (1995) Reproductive parameters of blue shark, Prionace glauca, and other sharks in the Gulf of Guinea. Marine and Freshwater Research 46, 967–973. Clarke, M. R., Clarke, D. C., Martins, H. R. and da Silva H. M. (1996) The diet of the blue shark (Prionace glauca L.) in Azorean waters. Arquipélago Life and Marine Sciences 14A, 41–56. Clarke, S. C. (2003) Quantification of the Trade in Shark Fins. Ph.D. thesis, Imperial College London, London, UK, 321 pp. Compagno, L. J. V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 2. Carcharhiniformes. FAO Fisheries Synopsis No. 125. FAO, Rome, Italy, pp. 251–655. Francis, M. P. and Duffy, C. (2005) Length at maturity in three pelagic sharks (Lamna nasus, Isurus oxyrinchus, and Prionace glauca) from New Zealand. Fishery Bulletin 103, 489–500. Gubanov, Ye. P. and Grigor’yev, V. N. (1975) Observation on the distribution and biology of the blue shark Prionace glauca (Carcharhinidae) of the Indian Ocean. Voprosy Ikhtiologii 15(1), 43–50 (in Russian). Hazin, F. H. V. (1993) Fisheries–Oceanographical Study on Tunas, Billfishes and Sharks in the Southwestern Equatorial Atlantic Ocean. Ph.D. thesis, Tokyo University of Fisheries, Tokyo, Japan, 286 pp. Hazin, F. H. V., Couto, A. A., Kihara, K., Otsuka, K. and Ishino, M. (1990) Distribution and abundance of pelagic sharks in the south-western equatorial Atlantic. Journal of the Tokyo University of Fisheries 77(1), 51–64. Hazin, F. H. V., Couto, A. A., Kihara, K., Otsuka, K., Ishino, M., Boeckman, C. E. and Leal, E. C. (1994) Reproduction of the blue shark Prionace glauca in the south-western equatorial Atlantic Ocean. Fisheries Science 60(5), 487–491. Henderson, A. C., Flannery, K. and Dunne, J. (2001) Observations on the biology and ecology of the blue shark in the north-east Atlantic. Journal of Fish Biology 58, 1347–1358. Hueter, R. E. and Simpfendorfer, C. A. (2008) Case study: Trends in blue shark abundance in the western North Atlantic as determined by a fishery-independent survey. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Kohler, N. E. and Turner, P. A. (2008) Stock structure of the blue shark (Prionace glauca) in the North Atlantic Ocean based on tagging data. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Kohler, N. E., Casey, J. G. and Turner, P. A. (1998) NMFS Cooperative Shark Tagging Program, 1962–93: An atlas of shark tag and recapture data. Marine Fisheries Review 60(2), 1–87. Last, P. L. and Stevens, J. D. (1994) Sharks and Rays of Australia. CSIRO, Collingwood, Victoria, Australia. Lessa, R., Santana, F. M. and Hazin, F. H. (2004) Age and growth of the blue shark Prionace glauca (Linnaeus, 1758) off northeastern Brazil. Fisheries Research 66, 19–30. Manning, M. J. and Francis, M. P. (2005) Age and Growth of Blue Shark (Prionace glauca) from the New Zealand Exclusive Economic Zone. New Zealand Fisheries Assessment Report 2005/26. Ministry of Fisheries, Wellington, New Zealand, 52 pp.

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Matsunaga, H. and Nakano, H. (1999) Species composition and CPUE of pelagic sharks caught by Japanese longline research and training vessels in the Pacific Ocean. Fisheries Science 65(1), 16–22. Muñoz-Chápuli, R. (1984) Ethologie de la reproduction chez quelques requins de l’Atlantique nordest. Cybium 8(4), 1–14. Nakano, H. (1994) Age, reproduction and migration of blue shark in the North Pacific Ocean. Bulletin of the National Research Institute of Far Seas Fisheries 31, 141–256. Nakano, H. (1996) Historical CPUE of pelagic shark caught by Japanese longline fishery in the world. Document AC 13.6.1 Annex, information paper submitted to the thirteenth CITES Animals Committee, Prague, Czech Republic, 7 pp. Nakano, H. and Nagasawa, K. (1996) Distribution of pelagic elasmobranchs caught by salmon research gillnets in the North Pacific. Fisheries Science 62(6), 860–865. Nakano, H. and Seki, M. P. (2003) Synopsis of biological data on the blue shark Prionace glauca Linnaeus. Bulletin of the Fisheries Research Agency 6, 18–55. Nakano, H. and Watanabe, Y. (1992) Effect of high seas driftnet fisheries on blue shark stock in the North Pacific. In: Compendium of Documents Submitted to the Scientific Review of North Pacific High Seas Driftnet Fisheries, Vol. 1. Sidney, British Columbia, Canada, 11–14 June 1991, 15 pp. Nakano, H., Makihara, M. and Shimazaki, K. (1985) Distribution and biological characteristics of the blue shark in the central North Pacific. Bulletin of the Faculty of Fisheries, Hokkaido University 36(3), 99–113 (in Japanese with English abstract). Nakano, H., Takeuchi, Y. and Suzuki, Z. (1999) Long term impact of tuna fishery on the pelagic sharks. In: Book of Abstracts, ICES/SCOR Symposium on the Ecosystem Effects of Fishing. Montpellier, France, 15–19 March 1999, p. 45. Pratt, H. W. (1979). Reproduction in the blue shark, Prionace glauca. Fisheries Bulletin 77(2), 445–470. Sciarrotta, T. C. and Nelson, D. R. (1977) Diel behaviour of the blue shark, Prionace glauca, near Santa Catalina Island, California. Fishery Bulletin 75(3), 519–528. Simpfendorfer, C. A., Heuter, R. E., Bergman, U. and Connett, S. M. H. (2002) Results of a fisheryindependent survey for pelagic sharks in the western North Atlantic, 1977–1994. Fisheries Research 55, 175–192. Sivasubramaniam, K. (1963) On the sharks and other undesirable species caught by tuna longline. Records of Oceanographic Works in Japan 7(1), 73–85. Skomal, G. B. and Natanson, L. J. (2003) Age and growth of the blue shark (Prionace glauca) in the North Atlantic Ocean. Fishery Bulletin 101, 627–639. Snelson Jr., F. F., Roman, B. L. and Burgess, G. H. (2008) The reproductive biology of pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Stevens, J. D. (1975) Vertebral rings as a means of age determination in the blue shark (Prionace glauca L.). Journal of the Marine Biological Association of the United Kingdom 55, 657–665. Stevens, J. D. (1976) First results of shark tagging in the north-east Atlantic. Journal of the Marine Biological Association of the United Kingdom 56, 929–937. Stevens, J. D. (1984) Biological observations on sharks caught by sport fishermen off New South Wales. Australian Journal of Marine and Freshwater Research 35, 573–590. Stevens, J. D. (1990) Further results from a tagging study of pelagic sharks in the north-east Atlantic. Journal of the Marine Biological Association of the United Kingdom 70, 707–720. Stevens, J. D. (2000) The population status of highly migratory oceanic sharks. In: Getting Ahead of the Curve: Conserving the Pacific Ocean’s Tunas, Swordfish, Billfishes and Sharks (ed. K. Hinman). National Coalition for Marine Conservation, Leesburg, VA.

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Stevens, J. D. and McLoughlin, K. J. (1991) Distribution, size and sex composition, reproductive biology and diet of sharks from northern Australia. Australian Journal of Marine and Freshwater Research 42(2), 151–199. Stevens, J. D. and Wayte, S. S. (1999) A Review of Australia’s Pelagic Shark Resources. Final Report to the Fisheries Research and Development Corporation, Project 89/107. FRDC, Deakin West, Australian Capital Territory, Australia, 64 pp. Strasburg, D. W. (1958) Distribution, abundance, and habits of pelagic sharks in the Central Pacific Ocean. Fisheries Bulletin 138, 335–361. Suda, A. (1953) Ecological study of blue shark (Prionace glauca Linné). Bulletin of the Nankai Fisheries Research Laboratory 1(26), 1–11. Tanaka, S. (1984) Present status of fisheries biology. In: Elasmobranchs As Fisheries Resources (eds. T. Taniuchi and M. Suyama). Fisheries Series 49. Japanese Society of Scientific Fisheries, Kousei-sha Kousei-kaku, Tokyo, pp. 46–59. Taniuchi, T. (1990) The role of elasmobranchs in Japanese fisheries. In: Elasmobranchs As Living Resources: Advances in the Biology, Ecology, Systematics, and Status of the Fisheries (eds. H. L. Pratt Jr., S. H. Gruber and T. Taniuchi). NOAA Technical Report NMFS 90. NOAA/ NMFS, Silver Spring, MD, pp. 415–426. West, G., Stevens, J. and Basson, M. (2004) Assessment of Blue Shark Population Status in the Western South Pacific. AFMA Project R01/1157. CSIRO Marine Research, Hobart, Tasmania, Australia, 139 pp. Wetherall, J. and Seki, M. (1992) Assessing impacts of North Pacific high seas driftnet fisheries on Pacific pomfret and sharks: Progress and problems. In: Compendium of Documents Submitted to the Scientific Review of North Pacific High Seas Driftnet Fisheries, Vol. 2. Sidney, British Columbia, Canada, 11–14 June 1991. Williams, F. (1977) Notes on the biology and ecology of the blue shark (Prionace glauca L.) in the eastern Pacific Ocean and a review of data from the world ocean. Unpublished report, 16 pp.

Chapter 13

The Biology and Ecology of the Pelagic Stingray, Pteroplatytrygon violacea (Bonaparte, 1832) Julie A. Neer

Abstract The pelagic stingray, Pteroplatytrygon violacea, has a circumglobal distribution in temperate and tropical seas. It is the only whiptail stingray known to inhabit the epipelagic waters of the ocean and is usually encountered in the upper ocean over deep water. Age estimates derived from vertebral sections indicate that pelagic stingrays live to be at least 10 years old. Variations in size at age and age at size were observed. Males are reported to mature between 37.5 and 47.8 cm disk width (DW). In the current study, all males examined were greater than 40 cm DW and were mature. Female maturity could not be more refined than the reported size of 40–50 cm DW. Captive data suggest that pelagic stingrays have between 4 and 13 young per litter, and timing of parturition may vary between the Pacific, Atlantic, and Mediterranean populations. Development is viviparous with uterolactation, with a gestation of 2–3 months. The diet of the pelagic stingray reflects its pelagic habitat, consisting of seahorses, squid, coelenterates, small teleost fishes, octopus, and crustaceans. Pelagic stingrays have been observed in the eastern and western Pacific, western Atlantic, and Indian Oceans, near the Lesser Antilles and Galápagos Islands, and in the northern Gulf of Mexico. There is no information regarding the stock structure of this species, and little is known of its movement patterns over most of its distribution. Although there is currently no directed fishing for this species, it is a common component of the bycatch of most pelagic longline fisheries for tunas, billfishes, and sharks. Key words: pelagic stingray, Pteroplatytrygon violacea, Dasyatidae, ageing study.

Introduction The pelagic stingray, Pteroplatytrygon (formerly Dasyatis) violacea (Bonaparte, 1832), is a medium-sized stingray of the family Dasyatidae and is the only whiptail stingray known to inhabit the epipelagic waters of the ocean (McEachran and Fechhelm, 1998). They are usually encountered in the upper ocean, often over deep water (Wilson and Beckett, 1970; Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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McEachran and Fechhelm, 1998). Previously thought to be exclusively pelagic, recent specimens collected at 330–381 m depth suggest that they may be a benthopelagic species, utilizing both benthic and pelagic habitats (Nakaya, 1982). There is currently no directed fishing for this species, although it is a common component of the bycatch of most pelagic longline fisheries for tunas, billfishes, and sharks.

Biology and ecology Little is known about the natural history of the pelagic stingray, mainly because of its preference for oceanic habitat. To address this lack of knowledge, an ageing study was conducted within the Southern California Bight region of the eastern Pacific Ocean. Eighty-three specimens of the pelagic stingray were collected in 1995 and 1996 as bycatch during the National Marine Fisheries Service/California Department of Fish and Game shark abundance indexing cruises. The surveys were conducted from June through August and targeted shortfin mako (Isurus oxyrinchus, Lamnidae), common thresher (Alopias vulpinus, Alopiidae), and blue shark (Prionace glauca, Carcharhinidae) using baited longlines. The specimens were weighed (kg) and measured (disk width, DW, in mm), reproductive information was collected, and a portion of the vertebral column was removed and frozen for age analysis. Specimens examined ranged from 411 to 565 mm DW for males (n
24) and 385 to 753 mm DW for females (n
57; Fig. 13.1). Two additional specimens (male
148 mm; female
118 mm) were obtained from an aborted litter from a ray held at the Monterey Bay Aquarium. 25 Female (n
58) Male (n
25)

Number of rays

20

15

10

5

750–799

700–749

650–699

600–649

550–599

500–549

450–499

400–449

350–399

300–349

250–299

200–249

150–199

100–149

0

Disk width (mm) Fig. 13.1 Length–frequency histogram of pelagic stingrays, Pteroplatytrygon violacea, collected during the 1995–1996 National Marine Fisheries Service/California Department of Fish and Game shark abundance indexing cruises in the Southern California Bight region (n
83).

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Vertebrae were prepared for age determination following Neer and Cailliet (2001). Cleaned vertebrae were measured (centrum diameter in mm) and embedded in epoxy resin, and a 0.4-mm sagittal section was cut from each. The sections were stained with 0.01% crystal violet to enhance band visibility following Carlson et al. (1999). Each section was mounted on a glass slide and examined under a compound microscope. Age determination using pelagic stingray vertebral sections was accomplished. Vertebrae growth appeared to be proportional to body growth as indicated by a significant relationship between centrum diameter and disk width (r2
0.6065; n
50), an underlying assumption for use of a hard body part as an ageing structure. Age estimates were determined by counting the number of growth bands observed on each section. Since no validation of the temporal component of the banding pattern was available, it was assumed that bands were deposited annually. Currently, three pelagic stingrays injected with oxytetracycline are being maintained at the Steinhart Aquarium in San Francisco, California, to assess this assumption. Age estimates were obtained for 43 specimens. Stingrays were determined to be between 2 and 10 years of age for females (n
30), and between 4 and 10 years for males (n
13; Fig. 13.2). Variation in both size at age and age at size was observed. If the age estimates are accurate, then two animals of the same length may be of different ages; this may have potential implications for the management of this species, should it become necessary. Growth curves could not be constructed for this species. Because of the small sample size for the age data (n
43), it would have been unwise to separate the data by sex. A von Bertalanffy growth curve was fitted to the combined data; however, the derived parameter estimates were unrealistic. The combined-sex model underestimated L, predicting a size considerably smaller than several of the specimens observed in the study.

900 800

Disk width (mm)

700 600 500 400 300 200 Female (n
30) Male (n
13)

100 0 0

2

4

6 8 Age estimate (years)

10

Fig. 13.2 Age estimates determined from pelagic stingray vertebral sections (n
43).

12

Biology and Ecology of the Pelagic Stingray

155

This result, coupled with the fact that pelagic stingrays display sexual dimorphism, indicates that a combined-sex growth model is inappropriate, and therefore meaningless for this species. Further research is needed to understand growth patterns in the wild. Growth data are available for pelagic stingrays in captivity. A study conducted at the Monterey Bay Aquarium in California determined that females had a faster growth rate than males, and that growth rates were seasonal in the captive environment (Mollet et al., 2002). Captive growth rates are most likely greater than what would be observed in the wild as the animals are fed to satiation daily. Reproductive data for this species are scarce. Only the left ovary and uterus are functional, as in other species of Dasyatis (Wilson and Beckett, 1970). Wilson and Beckett (1970), Mollet et al. (2002), and the author observed eggs encapsulated in a thin, semitransparent membrane within the uterus. The observed capsules contained, respectively, 13, between 2 and 7, and 5 egg segments. The current study observed 16 females with eggs, with an average of 6 eggs per female. Copulation is reported to take place between March and June in the northwestern Atlantic (Wilson and Beckett, 1970). Development in the pelagic stingray is viviparous with uterolactation (McEachran and Fechhelm, 1998). The embryos are nourished by protein-rich uterine milk (i.e., histotroph) via trophonemata from the uterine lining (Ranzi, 1934; Wilson and Beckett, 1970). Gestation time is 2–3 months, possibly the shortest of all elasmobranchs (Lo Bianco, 1909; Ranzi, 1934). Captive data suggest that pelagic stingrays have litters of 4–13 young, ranging from 14 to 24 cm at birth, and that ovulation in captivity may occur twice per year (Mollet et al., 2002). Parturition time appears to vary between the Atlantic, Pacific, and Mediterranean populations (Wilson and Beckett, 1970; Mollet, 2002). Size at sexual maturity in pelagic stingrays is uncertain. Wilson and Beckett (1970) reported that males and females reach sexual maturity between 40 and 50 cm DW. Additionally, males have been reported to mature from 37.5 cm DW (Tortonese, 1976) to 47.8 cm DW (McEachran and Fechhelm, 1998). The current study examined uterine width versus disk width for 53 female rays and found no clear indication of maturity (Fig. 13.3). Male sexual maturity was also examined by plotting clasper length versus disk width, along with the degree of clasper calcification (Fig. 13.4). All males examined (n
24; DW  40 cm) in this study were determined to be mature. For both sexes, the lack of immature samples (smaller than 40 cm DW) precluded the determination of size at first maturity for the eastern Pacific population. The diet of the pelagic stingray has not been well examined. The small amount of stomach content data indicate that the diet reflects its pelagic habitat. They feed on seahorses, squid, coelenterates (jellyfish and medusae), small teleost fishes, octopus, and crustaceans (Wilson and Beckett, 1970). Off California, they are known to seasonally pursue schools of mating squid (G. Zorzi, personal communication).

Distribution and movements The pelagic stingray appears to have a circumglobal distribution in temperate and tropical seas. Wilson and Beckett (1970) stated that they range in the western Atlantic Ocean from the Grand Banks and Flemish Cap to Cape Hatteras, North Carolina. Pelagic stingrays

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60

Uterine width (mm)

50

40

30

20

10

0 0

100

200

300

400

500

600

700

800

Disk width (mm) Fig. 13.3 Relationship of disk width to uterine width for the pelagic stingray (n
53). No clear indication of sexual maturity was observed.

90 80

Clasper length (mm)

70 60 50 40 30 20 Partial calcification (n
6)

10

Complete calcification (n
18)

0 0

100

200

300

400

500

600

Disk width (mm) Fig. 13.4 Relationship of disk width to clasper length for the pelagic stingray, with categories of clasper calcification (n
24). All specimens observed were determined to be mature.

Biology and Ecology of the Pelagic Stingray

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have also been observed in both the western and eastern Pacific Ocean, in the Indian Ocean, near the Lesser Antilles and Galápagos Islands, off Brazil, and in the northern Gulf of Mexico (Bigelow and Schroeder, 1962; Sadowsky and de Amorim, 1977; Nakaya, 1982; Branstetter and McEachran, 1983; McEachran and Fechhelm, 1998; Menni and Stehmann, 2000). New bycatch records indicate that pelagic stingrays can also be found in the waters of Australia, New Zealand, and Uruguay (Mollet, 2002; Domingo et al., 2005). For a more complete distribution discussion, see Mollet (2002). Currently, there is no information regarding the stock structure of this species. Little is known of the movement patterns of the pelagic stingray over most of its distribution. In the northwestern Atlantic Ocean, collections indicate movements north from the Gulf Stream in summer (June through September) when rays aggregate near the continental shelf (Wilson and Beckett, 1970). Specimens obtained from December through April were collected near or in Gulf Stream waters. These movements may be related to the warming of surface waters during summer (Wilson and Beckett, 1970). Some researchers have hypothesized that in the eastern Pacific Ocean, pelagic stingrays may be found far off the coast of Central America in winter, then move to higher latitudes closer to the coast in summer (Mollet, 2002).

Threats and status The population status of the pelagic stingray is unknown. There is currently no directed fishing for this species, although it is a common component of the bycatch of most pelagic longline fisheries (O’Brien and Sunada, 1994). As fishing effort offshore has increased, so has the number of rays taken incidentally in these fisheries, and the species currently appears to be far more abundant in offshore waters than previously reported. The major threats to the pelagic stingray population are the pelagic longline fisheries for tunas, billfishes, and other pelagic shark species. The national observer program onboard the Uruguayan tuna fleet observed 525 specimens of pelagic stingray on 13 trips between 1998 and 2001 (Domingo et al., 2005). Available data indicate that a significantly higher ratio of females to males is observed in the eastern Pacific and western Atlantic Oceans. Females outnumbered males 2:1 to 7:1 in the eastern Pacific samples and at a ratio greater than 3:1 for the western Atlantic (Wilson and Beckett, 1970; D. B. Holts, personal communication). Whether these ratios are obtained in actual fisheries bycatch is unknown; however, an asymmetric take of this species could potentially affect the long-term stability of pelagic stingray populations.

Conclusions This chapter presents the first age and growth estimates based on vertebral sections for the pelagic stingray. It also provides additional information regarding reproduction, as well as a summary of what is known about the general ecology and fishery importance of the species. Observed age estimates for the current study ranged between 2 and 10 years for females, and between 4 and 10 years for males. These are comparable to the data Schmid reported in

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1988, where he observed 2–9 bands for male and 6–12 bands for female Atlantic stingrays (Dasyatis sabina). Smith et al. (2003) stated that for the diamond stingray (D. dipterura), the maximum age, based on vertebral band counts, was 16.5 for males and 28 for females. These age estimates are higher than those found in the current study; however, Smith et al. covered the entire size range of the species concerned. Gestation time is reported to be 2–3 months for the pelagic stingray (Lo Bianco, 1909; Ranzi, 1934), which is considerably shorter than the gestation period reported for other dasyatid species. Henningsen (2000) reported that gestation in captive southern stingrays (D. americana) lasted 135–226 days (4.5–7.5 months), with a mean of 175.4  4.1 days (⬃6 months), while Struhsaker (1969) reported that gestation in the thorny stingray (D. centroura) takes 9–11 months, with pupping occurring in fall and early winter. Snelson et al. (1989) determined that bluntnose stingrays (D. sayi) mate in the spring, with parturition occurring approximately 1 year later, in middle May to early June. Captive information for pelagic stingrays indicates that they have litters of 4–13 young (Mollet et al., 2002). The present study found an average of six ova per female, which fits well with the published literature for Dasyatis species. Henningsen (2000) reported that litter size ranged from 2 to 10 pups, with an average of 4.2  0.3 pups, for captive southern stingrays. Struhsaker (1969) reported an average brood size of five pups per litter for the thorny stingray, and Snelson et al. (1989) observed broods of one to five pups for the bluntnose stingray. The pelagic stingray is an interesting pelagic batoid. It demonstrates some traits similar to those of other species in the family Dasyatidae, while sometimes having quite different characteristics. More research is needed to further examine these differences and similarities.

Acknowledgments I thank D. B. Holts, D. Ramon, the officers and crew of the NOAA ship David Starr Jordan, and the captains and crew of the R.V. Yellowfin for sampling support; and J. A. Coleman, A. Fischer, Moss Landing Marine Laboratories, and the Steinhart Aquarium for technical assistance. Thanks also to H. F. Mollet, J. B. O’Sullivan, J. M. Ezcurra, B. A. Thompson, and G. M. Cailliet for all the interesting discussions regarding these rays. Finally, thanks to the Ocean Wildlife Campaign and the Coastal Fisheries Institute of Louisiana State University for financial assistance that allowed me to participate in the International Pelagic Shark Workshop held in Pacific Grove, California.

References Bigelow, H. B. and Schroeder, W. C. (1962) New and little known batoid fishes from the western Atlantic. Bulletin of the Museum of Comparative Zoology, Harvard University 128(4), 159–244. Branstetter, S. and McEachran, J. D. (1983) A first record of the bigeye thresher, Alopias superciliosus, the blue shark, Prionace glauca, and the pelagic stingray, Dasyatis violacea, from the Gulf of Mexico. Northeast Gulf Science 6(1), 59–61.

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Carlson, J. K., Cortés, E. and Johnson, A. G. (1999) Age and growth of the blacknose shark, Carcharhinus acronotus, in the eastern Gulf of Mexico. Copeia 1999(3), 684–691. Domingo, A., Menni, R. C. and Forselledo, R. (2005) Bycatch of the pelagic ray Dasyatis violacea in Uruguayan longline fisheries and aspects of distribution in the southwestern Atlantic. Scientia Marina 69(1), 161–166. Henningsen, A. D. (2000) Notes on reproduction in the southern stingray, Dasyatis americana (Chondrichthyes: Dasyatidae), in a captive environment. Copeia 2000(3), 826–828. Lo Bianco, S. (1909) Notizie biologiche riguardanti specialmente il periodo maturita sessuale degli animalid del golfo de Napoli. Mitteilungen an der Biologischen Station zu Neapel 19, 35–691. McEachran, J. D. and Fechhelm, J. D. (1998) Fishes of the Gulf of Mexico, Vol. 1. University of Texas Press, Austin, TX. Menni, R. C. and Stehmann, M. F. W. (2000) Distribution, environment and biology of batoid fishes of Argentina, Uruguay and Brasil: A review. Revista del Museo Argentino de Ciencias Naturales, Nueva Serie 2(1), 61–109. Mollet, H. (2002) Distribution of the pelagic stingray, Dasyatis violacea (Bonaparte, 1832), off California, Central America, and worldwide. Marine and Freshwater Research 53, 525–530. Mollet, H., Ezcurra, J. M. and O’Sullivan, J. B. (2002) Captive biology of the pelagic stingray, Dasyatis violacea (Bonaparte, 1832). Marine and Freshwater Research 53, 531–541. Nakaya, N. (1982) Fishes of the Kyushu–Palau Ridge and Tosa Bay. Japan Fisheries Resource Conservation Association, Tokyo, Japan. Neer, J. A. and Cailliet, G. M. (2001) Aspects of the life history of the Pacific electric ray, Torpedo californica (Ayres). Copeia 2001(3), 842–847. O’Brien, J. W. and Sunada, J. S. (1994) A review of the southern California experimental drift longline fishery for sharks, 1988–1991. California Cooperative Oceanic Fisheries Investigations Report 35, 222–229. Ranzi, S. (1934) Le basi fisio-moriologiche dello sviluppo embrionale dei selaci. Part 2. Pubblicazioni della Stazione Zoologica di Napoli 13, 331–437. Sadowsky, V. and de Amorim, A. F. (1977) Primeiro registro de ocorrência da arraia pelágica Dasyatis violacea (Bonaparte, 1832) nas agues do Atlántico Sul Occidental. Ciencia e Cultura, Supl. Resumos 29(7), 792. Schmid, T. H. (1988) Age, Growth, and Movement Patterns of the Atlantic Stingray, Dasyatis sabina, in a Florida Coastal Lagoon System. Master’s thesis, University of Central Florida, College of Arts and Sciences, Orlando, FL, 85 pp. Smith, W. D., Cailliet, G. M. and Mariano Melendez, E. (2003) Aspects of the life history and population structure of the diamond stingray, Dasyatis dipterura. Abstract from the 83rd Annual Meeting of the American Society of Ichthyologists and Herpetologists, Manaus, Brazil, June 2003. Snelson, J., Franklin, F., Williams-Hooper, S. E. and Schmid, T. H. (1989) Biology of the bluntnose stingray, Dasyatis sayi, in Florida coastal lagoons. Bulletin of Marine Science 45(1), 15–25. Struhsaker, P. (1969) Observations on the biology and distribution of the thorny stingray, Dasyatis centroura (Pices: Dasyatidae). Bulletin of Marine Science 19(2), 456–481. Tortonese, E. (1976) A note on Dasyatis violacea (BP) (Plagiostomia, Rajiformes). Bolletino di Pesca Piscicoltura e Idrobiologia 31, 5–8. Wilson, P. C. and Beckett, J. S. (1970) Atlantic Ocean distribution of the pelagic stingray, Dasyatis violacea. Copeia 1970(4), 696–707.

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Part III

Trends in Catches and Abundance of Pelagic Sharks

Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Introduction Although the sharks of the open ocean have received limited research attention from biologists, fishermen have been catching these sharks, both inadvertently and deliberately, in large numbers since the rise of high-seas fishing in the 1950s. Information from logbooks and observers on high-seas fishing vessels can potentially be used to infer the trends and status of open ocean shark populations. In addition, historical catches provide some information about both abundance and the impact of fisheries on these sharks. The chapters in this section evaluate catch and catch-rate data by ocean, by fishing nation, and for several fisheries around the world, and offer insight into current trends in abundance.

Description of fisheries and catch data Pelagic sharks are caught in commercial fisheries throughout the world’s oceans. In general, landings and discards are poorly documented at the species level, complicating management efforts and our ability to identify the most important pelagic-shark-fishing nations (Chapters 14 and 21). According to United Nations Food and Agriculture Organization (FAO) statistics, elasmobranch catches in the Pacific and Indian Oceans are comparable to catches in the Atlantic, but more species-specific catch records are available for the Atlantic. Although landings in the FAO database have increased since the 1990s, it is difficult to determine whether this represents an actual increase in shark catches or just better reporting. Pelagic sharks, including blue (Prionace glauca), silky (Carcharhinus falciformis), and mako (Isurus spp.) sharks, are commonly taken as bycatch in high-seas longline fisheries. These sharks are often discarded because they have little value compared to the tuna (Scombridae) and swordfish (Xiphias gladius) that are the target species, although their fins are retained for the lucrative shark fin market (Chapter 17). From US pelagic longline observer data, dead discards of pelagic sharks, including many juvenile silky, night (Carcharhinus signatus), and bigeye thresher (Alopias superciliosus) sharks, are substantial (Chapter 20). Some fisheries have traditionally targeted sharks for their meat, such as artisanal, pelagic longline, and gill-net fisheries along the Pacific Coast of Mexico that target blue, thresher (Alopias spp.), and other sharks. New management measures to conserve these culturally important shark resources, which are apparently being fished at or above sustainable levels, were implemented in 2007 (Chapter 24). Fisheries in Brazil and Uruguay sometimes target pelagic sharks, depending on market conditions (Chapter 17). The developing market for blue shark meat in Spain has increased the targeting of blue sharks around the Azores, as a seasonal complement to the swordfish fishery (Chapter 18). Seasonal shifts to target pelagic sharks when traditional species are not available also occur in the Gulf of California (Chapter 24). Sport fisheries for pelagic sharks occur around the world, although they have little impact on shark populations compared to the commercial fisheries (Chapter 15). The trend toward catch-and-release fishing has reduced the number of pelagic sharks killed by sportfishing in the last decade, and as in commercial fisheries, blue sharks are the most commonly caught pelagic sharks, but shortfin mako and thresher sharks are more often targeted.

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Abundance trends from catch-rate data Catch per unit effort (CPUE) is frequently used as an indicator of abundance. This measure assumes that the total catch of sharks is proportional to both the biomass of sharks in the ocean and the amount of fishing effort (Hilborn and Walters, 1992): C
qEB where B is the biomass of sharks available to the fishery, C is catch (in weight), E is fishing effort (e.g., the number of hooks, sets, or vessel days), and q, called catchability, is the constant of proportionality. If the catchability is constant over time, then the CPUE is C/E
qB and CPUE (e.g., average catch per set) will follow the same trend as abundance. CPUE is most likely to be proportional to abundance for scientific survey data, in which the fishing methodology is constant over time and fishing locations are randomly or systematically distributed. Unfortunately, few surveys have been conducted on the high seas, although some open ocean sharks are caught in surveys in coastal waters (Chapter 19). More often, CPUE data from fishery logbooks or from at-sea observers on fishing vessels are used to infer abundance trends for pelagic sharks. For fishery CPUE, catchability can change if the fisheries change their gear, spatial distribution, fishing methodology, or target species. Changes over time in reporting practices can also result in bias in abundance trend estimates. To extract an unbiased index of abundance from fishery CPUE data, it is generally necessary to estimate the impacts of gear type and other factors on CPUE, so that these impacts can be removed from the estimated biomass trend. This is generally done by modeling CPUE as a function of the factors that influence catchability using a generalized linear model (GLM). Such models estimate the effect of explanatory variables, such as spatial location and gear type, so that their effects can be removed from the estimated annual CPUE. The resulting standardized year effect is then an index of abundance. The estimated abundance trend may still be incorrect if there are factors for which no data are available, for example, when information is lacking for changes over time regarding whether fishers record shark catches. Despite these well-known problems (e.g., Walters, 2003), for many open ocean sharks, CPUE are the only data available from which to infer abundance trends. In the North Atlantic, the available CPUE data generally show a declining trend for shortfin mako sharks, and no trend or conflicting trends for blue sharks (Chapters 30 and 37). Chapter 19 presents evidence for a significant decline in male blue sharks from a fishery-independent research longlining operation in the Northwest Atlantic between 1977 and 1994. Chapter 18 used a GLM model to evaluate blue shark logbook CPUE data from the Portuguese longline fleet operating around the Azores, and found an increasing trend over time, which was attributed to increased targeting of blue sharks. Indices derived from recreational fisheries on the US Atlantic Coast, and shark tournaments in Massachusetts, are highly variable and show no trend (Chapter 16). For mako sharks, there appeared to

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be a declining trend in the Massachusetts tournament data, but recent years have shown an increasing trend. In the South Atlantic, blue shark trends are also contradictory, whereas populations of shortfin mako are declining (Chapter 37). For the fisheries of Brazil and Uruguay, most of the annual variation in shark CPUE can be attributed to changes in targeting and discarding of sharks driven by changes in markets for shark meat (Chapter 17). For blue sharks in this region, some of the fine-scale temporal and spatial patterns in the catch rates can be explained by a hypothesized migration of sharks throughout their reproductive cycle. Few catch-rate series are available for the Pacific and Indian Oceans, mostly from highseas longline fisheries of Japan and the United States. In the US fisheries taking pelagic sharks in the western Pacific, both catches and catch rates of pelagic sharks have declined since 1993, possibly reflecting changes in fishing methodology (Chapter 23). Chapter 22 describes both the historical Japanese longline fishery and recent domestic longline fishery in Australian waters. These catches are dominated by blue sharks, particularly farther south, although silky sharks are also taken. There was no obvious trend in blue shark catch rates over time in this fishery.

Recommendations Existing fishery-dependent data provide useful information about the biology, distribution, and abundance of open ocean sharks, but improved management of these species will require more accurate catch data. Marine reserves or time and area closures may contribute to the protection of vulnerable species and life stages of open ocean sharks, but the design of these measures will require more data from at-sea observers on the seasonal and spatial distribution of shark catches by species, age, and sex.

References Hilborn, R. and Walters, C. J. (1992) Quantitative Fisheries Stock Assessment: Choice, Dynamics and Uncertainty. Chapman & Hall, London, UK. Walters, C. (2003) Folly and fantasy in the analysis of spatial catch rate data. Canadian Journal of Fisheries and Aquatic Sciences 60, 1433–1436.

Chapter 14

A Global Overview of Commercial Fisheries for Open Ocean Sharks Merry D. Camhi, Elizabeth Lauck, Ellen K. Pikitch and Elizabeth A. Babcock

Abstract Pelagic sharks are caught throughout the Atlantic, Pacific, and Indian Oceans, and total elasmobranch catches reported to the Food and Agriculture Organization averaged around 261,000 metric tons (t) per ocean basin per year from 1988 to 2002. Reported chondrichthyan catches increased during the 1980s and 1990s, particularly in the Indian Ocean, although the increase may be partially explained by improved data collection. In 2002, only 26% of the chondrichthyan catches in the Atlantic, 11% in the Pacific, and 7% in the Indian Ocean were identified to species. Of the identified catches, 28% in the Atlantic, 23% in the Pacific, and 55% in the Indian Ocean were of pelagic sharks. Few fishing nations report the species composition of their shark catches or landings, obscuring which countries are engaged in pelagic shark fishing and, thus, where management efforts are needed. However, on the basis of total reported elasmobranch landings, the size of tuna and billfish fisheries, and importance in the Hong Kong shark fin trade, as well as other factors, the following countries are believed to be responsible for the majority of the world’s pelagic elasmobranch landings: Brazil, Indonesia, Japan, Mexico, Pakistan, Republic of Korea, Spain, Sri Lanka, Taiwan, and the United States. This chapter summarizes what is known about pelagic shark fisheries by ocean basin and for the 22 major shark-fishing nations, which together accounted for 82% of the global elasmobranch landings (843,413 t) in 2002, and highlights gaps, problems, and inconsistencies in the shark catch data that make it difficult to evaluate the impact of fisheries on open ocean sharks. Key words: commercial fisheries, pelagic sharks, elasmobranchs, bycatch, data collection, trade, shark fins, Prionace, Isurus, Lamna, Carcharhinus, Alopias, Carcharodon.

Introduction Pelagic sharks are among the world’s most cosmopolitan marine animals, occurring in every ocean basin and across most latitudes. The pelagic elasmobranch species considered in this volume are frequently encountered in open ocean fisheries, and are probably taken Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Table 14.1 Pelagic shark species in the international trade in shark meat, fins, skin, and oil.a Scientific name Alopias pelagicus Alopias superciliosus Alopias vulpinus Carcharodon carcharias Isurus oxyrinchus Isurus paucus Lamna ditropis Lamna nasus Carcharhinus falciformis Carcharhinus longimanus Prionace glauca Pteroplatytrygon violacea

Common name

Meat

Finsb

Pelagic thresher Bigeye thresher Common thresher White Shortfin mako Longfin mako Salmon Porbeagle Silky Oceanic whitetip Blue Pelagic stingray

冑 冑 冑+

冑(2.3%) 冑 冑 冑 冑(2.7%) 冑 冑 冑 冑(3.5%) 冑(1.8%) 冑(17.3%)

冑+ 冑 冑+ 冑

Skin c

冑 冑 冑 冑 冑+ 冑+ 冑+ 冑

Liver oil

冑 冑 冑 冑+ 冑 冑 冑 冑

冑: frequently used; 冑: preferred species. From Rose (1996) and Clarke et al. (2005). Percentage of world trade (in parantheses) is based on proportions in the Hong Kong shark fin market (Clarke et al., 2006b). c Percentage for all three thresher species.

a

b

intentionally or as bycatch by most fishing nations. The shortfin mako (Isurus oxyrinchus, Lamnidae), thresher (Alopias spp., Alopiidae), porbeagle (Lamna nasus, Lamnidae), salmon (L. ditropis, Lamnidae), silky (Carcharhinus falciformis, Carcharhinidae), oceanic whitetip (C. longimanus, Carcharhinidae), and blue (Prionace glauca, Carcharhinidae) sharks are all known to be targeted by fisheries in various oceans of the world (Vannuccini, 1999). Fisheries that target sharks are mainly driven by markets for shark fins and, in some cases, shark meat, although shark skin and liver oil are also marketed (Table 14.1). In addition, all pelagic elasmobranchs, including the white shark (Carcharodon carcharias, Lamnidae) and the pelagic stingray (Pteroplatytrygon violacea, Dasyatidae), are taken as bycatch in fisheries targeting other species, especially by high-seas longline vessels targeting tuna and swordfish (Bailey et al., 1996; Camhi et al., 1998). While pelagic sharks are almost always classified as bycatch, they often represent a significant, if not dominant, portion of a vessel’s catch. Although sharks have traditionally been discarded because of the relatively low ex-vessel value of their flesh, growing international markets and high prices paid for shark fins have increased retention rates of pelagic sharks, or at least of their fins (Camhi, 1999; Pawson and Vince, 1999). Pelagic shark fins are reported to fill gaps in fishing income for high-seas fisheries when more lucrative tuna and swordfish catches are down or simply to provide additional revenue for fishing crews (Bailey et al., 1996; Aires-da-Silva et al., 2008). The increasing demand and prices paid for fins (Clarke, 2004) may help explain stable or ongoing growth in global shark catches despite local population depletions. This chapter examines available catch and landings data for pelagic sharks, with a focus on the data limitations that undermine our ability to effectively manage shark fisheries, and summarizes the pelagic shark fisheries of the top shark-fishing nations.

Data limitations and collection efforts Although pelagic sharks may dominate the catch in many open ocean fisheries, collecting data on these catches has been difficult for several reasons. First, management agencies that

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struggle to monitor and manage fisheries for target species have been reluctant to commit management resources to bycatch species in the absence of national or international mandates (Alverson et al., 1994), especially for species that have been traditionally of low economic importance (Bonfil, 1994; Rose, 1996). Even where shark landings are monitored, most countries fail to record species or even groups in their landings data, often referring to sharks landed as only “large” or “small” (e.g., Taiwan and Mexico), or simply “sharks.” For developing nations, catches are difficult to estimate because data are frequently lacking from artisanal fisheries, as well as for foreign longline fleets with access rights (Barnett, 1997). In 1994, in recognition of these data problems, the Convention on International Trade in Endangered Species (CITES) called on member countries to begin collecting biological and fisheries information on the trade in shark products (CITES, 1994). In 1999, to help member countries meet the requirements of the Code of Conduct for Responsible Fisheries, the Food and Agriculture Organization (FAO) of the United Nations adopted an International Plan of Action (IPOA) for Sharks (FAO, 1999), which requests that fishing nations and regional fishery management organizations (RFMO) voluntarily assess and manage their target and bycatch shark fisheries (Cavanagh et al., 2008). The FAO collects global statistics of marine fisheries catches. Data are voluntarily submitted to FAO by about 125 shark-fishing countries. The database, however, is only as good as the data received from these countries. Although the FAO database may be the most exhaustive for global shark fisheries, it is widely acknowledged that actual elasmobranch catches (sharks and rays) may be twice as high as indicated by the FAO figures because of poor record-keeping, lack of reporting, and deliberate underreporting (Bonfil, 1994; Watson and Pauly, 2001; Clarke et al., 2006a). Of the 100 or so chondrichthyans that are regularly encountered in commercial fisheries, in 2002 FAO reported catches for 65 species, including 8 pelagic species (common thresher (Alopias vulpinus), bigeye thresher (A. superciliosus), silky, shortfin mako, longfin mako (Isurus paucus), porbeagle, white, and blue). However, only 15% of the total shark, ray, and chimaera catch in 2002 was identified to species (26% in the Atlantic, 11% in the Pacific, and 7% in the Indian Ocean; FAO, 2006). More often, elasmobranch landings are amalgamated under the general heading “sharks” or “sharks, rays, other.” Some major shark-fishing nations such as Brazil, Portugal, and Spain do report at least some pelagic shark landings identified to the species level. Yet these FAO landings are clearly incomplete, and can be used only to suggest relative catch level by ocean for those reporting countries. For example, only 33 metric tons (t) of blue sharks were reported from the Pacific in 1994, whereas Stevens (2000) estimated that 140,000 t of blue sharks were taken from Pacific high seas in the same year. Despite these limitations, the FAO database (FAO, 2003a, 2006) is a helpful starting point for an evaluation of global fisheries for open ocean sharks. Landings statistics can also be supplemented by trade and market data to provide a more complete picture of shark exploitation worldwide. Hong Kong is the hub of the international trade in shark fins, and between 50% and 85% of the world’s shark fins are exported to Hong Kong from about 86 countries (Vannuccini, 1999; Clarke, 2002, 2004). An analysis of trade data from Hong Kong shark fin auctions found that pelagic sharks represent a significant proportion of sharks in the international fin trade (Clarke, 2003; Clarke et al., 2005, 2006a, b). Using DNA forensic methodology, Clarke et al. (2006b) estimated that pelagic sharks account for about one-third of the fins traded in Hong Kong,

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although they were unable to identify 54% of the shark fins in the market (implying that the actual percentage could be higher). Projections of world fin trade data from this survey also suggest that FAO data may significantly underestimate global shark mortality. In addition, CITES provides data on the exploitation of listed species in international trade. In October 2004, the white shark was listed on CITES Appendix II; this listing now requires the 169 member countries to monitor trade in white shark products and to ensure that the trade is not jeopardizing the status of the species. New elasmobranch working groups and data collection programs established by the International Commission for the Conservation of Atlantic Tunas (ICCAT) and the International Council for the Exploration of the Sea (ICES) will serve as a helpful supplement to the FAO database for Atlantic fisheries. In November 2004, ICCAT became the first RFMO to adopt a recommendation (No. 04-10) requiring all member and cooperating nations to submit total catches and landings (including estimates of dead discarded catch) of pelagic sharks, especially for porbeagle, mako, and blue sharks. These data now represent the most complete database currently available on pelagic shark catches by ocean basin (ICCAT, 2006). However, although Atlantic fisheries are probably the best documented because of ICCAT’s efforts (see Babcock and Nakano, 2008), underreporting of catches remains a major challenge to pelagic shark assessments and management (ICCAT, 2005). A similar effort to collect shark catch and bycatch data is being undertaken in the Pacific under the auspices of the Secretariat of the Pacific Community (SPC). Because the central and western Pacific Ocean are home to the largest industrial tuna fishery in the world (Williams, 1999), gaining a better understanding of the number and species of sharks being killed in Pacific Ocean fisheries should be a top priority for their conservation and management. The newly formed Western and Central Pacific Fisheries Commission (WCPFC) has convened a working group on ecosystems and bycatch, with a mandate to evaluate the impacts of the tuna fisheries in the WCPFC region on nontarget species, including sharks (WCPFC, 2006). Information on shark bycatch in the eastern tropical Pacific is available from the Inter-American Tropical Tuna Commission (IATTC) observer program (RománVerdesoto and Orozco-Zöller, 2005). There is no RFMO collecting data on sharks in the northern Pacific, although some fishing nations in the region record shark catches. In the Indian Ocean, the Indian Ocean Tuna Commission (IOTC) serves as a regional data collection organization for high-seas tuna fisheries. The IOTC Working Group on Bycatch met for the first time in July 2005 and acknowledged that, despite calls for speciesspecific reporting of both catches and discards for all bycatch species (including sharks), few Indian Ocean fishing countries submit these data (IOTC, 2005a). However, Resolution 05/05 adopted in 2005, which directs all IOTC members and cooperating parties to report shark landings to IOTC and bans the practice of finning, should help close the information gap in the Indian Ocean (IOTC, 2005b). One goal of this chapter is to evaluate which nations are responsible for the majority of pelagic shark catches. However, the incomplete data on pelagic shark landings and discards in most of the world’s oceans precluded a strictly quantitative analysis of the number of pelagic sharks taken annually in fishing operations. Instead, qualitative descriptions of domestic fisheries in the published literature informed the following country overviews and rankings. We reasoned that the major shark-fishing nations that (1) are members of RFMOs with oversight for high-seas tuna and billfish fisheries (see Camhi et al., 2008),

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1,000,000

Atlantic

Indian

Pacific

Catch (t)

750,000

500,000

250,000

2000

1995

1990

1985

1980

1975

1970

1965

1960

1955

1950

0

Year

Fig. 14.1 Reported catches of elasmobranchs by ocean basin, from FAO catch statistics (FAO, 2006).

(2) have distant-water fleets, (3) are among the top shark fin exporters to Hong Kong, and/ or (4) report pelagic shark landings to FAO are also likely to account for significant pelagic shark catches and mortality. Where possible, we focused on catches in 2002, because these catch data should be complete in the FAO and RFMO databases, while recent data are more likely to be incomplete or subject to revision.

Global elasmobranch catches FAO reports that 4,275,000 t of elasmobranchs were caught in the Atlantic Ocean between 1988 and 2002, for an average catch of 285,000 t/year. During the same period, 3,993,000 t were reported from the Pacific (266,000 t/year) and 3,466,000 t from the Indian Ocean (231,000 t/year; Fig. 14.1; FAO, 2003a, 2006). Most of these elasmobranch catch data are not species specific: In 2002, of reported elasmobranch landings that were identified to species, 28% in the Atlantic, 23% in the Pacific, and 55% in the Indian Ocean were of pelagic sharks (Table 14.2). Worldwide elasmobranch catches increased by about 2% annually between 1988 and 2002 (Fig. 14.1), although they appear to have stabilized since the mid-1990s. The total catch was 843,413 t in 2002 (FAO, 2003a, 2006). It is estimated that approximately 60% of the elasmobranch catches reported to FAO – about a half million t in 2002 – are sharks, the remainder being skates and rays (Bonfil, 1994). Since the mid-1990s, four regions – western-central Pacific, western Indian Ocean, eastern Indian Ocean, and Northeast Atlantic – have been responsible for the majority of FAO-reported elasmobranch landings; together they contributed 50% of the global landings in 2002 (FAO, 2003a, 2006). Hong Kong trade data indicate a world trade in shark fins of 11,000 t in 2000, which suggests that the shark biomass needed to support the global fin trade each year ranges from 1.21 to 2.29 million t, or 26–73 million sharks (Clarke et al., 2006a). These estimates reveal that the shark biomass represented in the fin trade is three to four times

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Table 14.2 Pelagic sharks as identified in the FAO database by reported landings (t) by ocean basin in 2002 (FAO, 2006).a Species or species group

Scientific name

Bigeye thresher Common thresher Thresher shark nei White Shortfin mako Longfin mako Mako sharks nei Porbeagle Silky Oceanic whitetip Blue

Alopias superciliosus Alopias vulpinus Alopias spp. Carcharodon carcharias Isurus oxyrinchus Isurus paucus Isurus spp. Lamna nasus Carcharhinus falciformis Carcharhinus longimanus Prionace glauca

Subtotal pelagics Pelagics identified to species Total elasmobranchs identified to species Total elasmobranchs

Atlantic Ocean 0 58 0 0 3,374 1 37 807 70 0 16,511

Pacific Ocean

Indian Ocean

Total

0 406 454 0 1,860

381

80 203 1,484

0 6,830

3,678

3,304

464 454 0 5,615 1 117 1,010 8,384 0 23,493

20,858 20,821 73,540

8,165 7,631 33,456

10,515 10,515 19,104

39,538 38,967 126,100

283,155

291,071

268,559

843,413b

a Additional pelagic landings are likely included in such amalgamated categories as “sharks, rays, skates, etc., nei” and “various sharks nei” (nei
not elsewhere indicated); these landings are included here in “total elasmobranchs.” A reported catch of zero means that the species has been reported in that ocean, but the catch in 2002 was less than 1 t. b Total includes 628 t of unidentified sharks and rays caught in the Southern Ocean.

higher than shark catch figures reported to FAO. Yet these numbers likely underestimate the actual mortality because fins that are consumed domestically are not recorded in the trade statistics, and underreporting and black markets are widespread. In the Hong Kong market sample, blue (17.3%) and silky (3.5%) sharks were the largest contributors, followed by shortfin mako (2.7%), thresher (2.3%), and oceanic whitetip (1.8%) sharks (Clarke et al., 2006b), which suggests that 7–24 million pelagic sharks are used to support the fin trade each year (S. Clarke, personal communication). The prevalence of these species in the Hong Kong fin market also suggests that pelagic sharks may account for a significant proportion of the fin exports from the top fin-exporting nations. Although extensive transshipments of fins make it difficult to trace the waters and countries of origin, fin trade data may help corroborate a country’s importance as a pelagic shark-fishing nation. In 1999, Spain was, by far, the top exporter of fins to Hong Kong, reporting exports of more than 2 million t, or 27% of the world total (Table 14.3; Clarke and Mosqueira, 2002). Other major elasmobranch-fishing nations that ranked among the top 20 fin exporters to Hong Kong in 1999 were the United States, Taiwan, Indonesia, Japan, India, Mexico, Brazil, Peru, and Canada. In more recent years (2001– 2005), however, Mainland China has led in fin exports to Hong Kong, followed by United Arab Emirates (UAE), Spain, Taiwan, Singapore, Indonesia, Brazil, Mexico, Japan, and Costa Rica, although UAE and Singapore are re-export sites rather than producers of fins (Anonymous, 2006). Fin imports into Hong Kong rose at an annual rate of 6.1% from 1991 to 2000 (Clarke, 2004).

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Table 14.3 The 22 major shark-fishing nations in 2002, their FAO landings, and characteristics of their fisheries, including directed or incidental fisheries for pelagic sharks, distant-water fleets, and importance in Hong Kong shark fin imports. Country

2002 FAO elasmobranch landings (t)

Indonesia India Spain Pakistan Taiwan Japan Mexico New Zealand Argentina Sri Lanka Malaysia United States France Thailand Brazil United Kingdom Peru Portugal Nigeria Canada Korea, Republic of Maldives

106,398 66,923 62,996 49,904 44,412 32,879 30,888 30,208 26,251 25,340 24,167 24,076 23,136 21,736 21,238 16,832 16,633 14,016 13,449 13,144 11,961 11,498

Subtotal (82% of 2002 total)

688,085

Pelagic shark fisheriesa

D, I I D, I D?, I D, I D?, I D, I I I D, I I D, I D, I I D, I D, I D?, I D, I D?, I D, I D, I D, I

Distant-water fleets (103 t)b

Atlantic, Med  Indian (22,860) Worldwide (7,370) Worldwide (49,569) Pacific (89) Pacific (0.176) Atlantic (4) Indian (30) Atlantic  Pacific (2,254) Atlantic  Pacific (6,044) Indian  South China Sea Atlantic (14) Atlantic (696) Pacific (48) Atlantic (7,095) Atlantic (16) Atlantic (101) Worldwide (11,086)

Rank in fin exports to Hong Kong (1999)c 4 8 1 28 3 6 9 34 27 23 38 2 69 54 11 na 13 62 52 20 65 66

a

D: pelagic sharks are targeted; I: pelagic sharks are taken incidentally. Defined as fleets fishing outside of country’s EEZ; cumulative catches of all fishes from 1950 to 1994 outside of their own FAO Statistical Area are given in parentheses (Bonfil et al., 1998). c From Clarke and Mosqueira (2002). na: not applicable. b

Pelagic sharks in Atlantic Ocean fisheries In the Atlantic Ocean, pelagic sharks are caught primarily as bycatch in fisheries for tuna and swordfish, although they may be increasingly targeted in some of these fisheries (Aires-da-Silva et al., 2008). According to the FAO database, catches of all elasmobranchs in the Atlantic were between 250,000 and 340,000 t/year between 1988 and 2002. In 2002, of the Atlantic-wide elasmobranch catch of 283,155 t, 73,540 t could be identified to species, of which about 28% were pelagic sharks, primarily blue sharks (Table 14.2). The ICCAT database includes 52 shark species, and for the period 1980–2005, pelagic sharks made up about 67% of the reported shark catches. This high percentage of pelagic sharks in part reflects the fact that some nations do not report catches of coastal sharks to ICCAT or began reporting coastal shark catches only in the mid-1990s (ICCAT, 2005). Blue sharks represented 73% of the total catch of pelagic sharks by weight between 1980 and 2005, followed by shortfin mako, which accounted for 17% (ICCAT, 2006). These

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80,000 70,000

Blue Makos Porbeagle

Catch (t)

60,000 50,000

Other pelagic

40,000

Other and unidentified

30,000 20,000 10,000 2001

1996

1991

1986

1981

0

Year Fig. 14.2 Reported catches of pelagic sharks by species in the Atlantic Ocean, from ICCAT catch statistics (ICCAT, 2006). “Makos” includes shortfin mako and longfin mako shark. “Other pelagic” includes silky, oceanic whitetip, thresher and white sharks, as well as catches reported as pelagic shark not elsewhere indicated. “Other and unidentified” includes sharks that were not identified and sharks identified as coastal taxa.

two species and porbeagle made up 97% of the total catch of pelagic sharks during this period (Fig. 14.2). The ICCAT database reports a total of 347,646 t of blue shark landings, which can be divided into three distinct phases over the past 25 years (ICCAT, 2006). From 1981 through 1993, the US blue shark catch averaged 785 t/year, while France reported an average catch of 106 t. In 1994, Japan started to report blue shark landings to ICCAT, dwarfing those of the United States (601 t) and France (350 t) with a catch of 2,596 t. In 1997, Spain started reporting blue shark landings, with a catch of more than 29,000 t in 1999. Since 1997, Spain has reported the greatest number of blue sharks, accounting for 70% of total Atlantic blue shark landings. Spain is also a leading exporter of shark meat, primarily to other European countries, as well as a leading supplier of unprocessed shark fins to the Hong Kong shark fin market (Clarke and Mosqueira, 2002). Portugal accounts for 14% of reported blue shark landings from the Atlantic for the period 1997–2005, followed by Brazil (4%), Namibia (4%), and Japan (3%). According to the ICCAT database, the shortfin mako is the second most numerous pelagic shark in the Atlantic landings, with 80,996 t reported between 1980 and 2005, for an average of 3,115 t/year. Shortfin mako catches have increased gradually since 1980 to a high of 7,462 t in 2004 (in Fig. 4.2, 98% of the makos reported are shortfin makos). Over this period, Spain landed 32% of the shortfin mako caught in the Atlantic Ocean, followed by Japan (24%), the United States (19%), and Portugal (13%). While the flesh and fins of blue, mako, thresher, and silky sharks are marketable, these species are not the primary target of most of the Atlantic fisheries that land them. By contrast, the highly prized flesh of porbeagle sharks has made this species a target of intensive fisheries (Castro et al., 1999). Total porbeagle landings between 1980 and 2005 in the ICCAT database were 32,955 t (1,268 t/year), or 7% of total pelagic shark landings over that period. Canada reported 36% of that catch, France 32%, the Faroe Islands 19%, Denmark 6%, and Norway 3%. Porbeagle catches steadily increased into the mid-1990s, peaking in 1994 at 2,676 t before declining to 556 t in 2005.

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Between 1980 and 2005, ICCAT reported 3,145 t of silky shark catches, and 1,921 t of oceanic whitetip sharks. Reported catches of silky sharks ranged from 13 t (1991) to 553 t (1996) with no clear trend. Catches of oceanic whitetip sharks have been higher since 1999 than in any other period, with a maximum of 642 t in 2000. The large recent landings of silky and oceanic whitetip sharks are of concern given indications of their probable highly depleted status in the Atlantic Ocean (Baum et al., 2003; Baum and Myers, 2004).

Pelagic sharks in Pacific Ocean fisheries Pelagic sharks are captured primarily as bycatch in Pacific Ocean fisheries for tunas, swordfish, and marlins. The Pacific Ocean is home to the world’s largest industrial tuna fishery (Bailey et al., 1996) and, as in tuna fisheries in the Atlantic, catch of pelagic sharks is common. Data collection programs to document encounters with bycatch species, such as sharks, are limited in Pacific Ocean fisheries and few data are available to the species level; thus, the overall oceanwide picture is even less clear than in the Atlantic. On a broad scale, the FAO database reveals that Pacific catches of all elasmobranchs fluctuated between 250,000 and 290,000 t/year between 1988 and 2002 (Fig. 14.1). Assuming that 60% of these reported landings are sharks (Bonfil, 1994), approximately 175,000 t of sharks were taken from Pacific waters in 2002. Of the shark catches reported to the FAO from the Pacific Ocean, more than half were taken in the western-central Pacific, in the area largely covered by the SPC as well as the WCPFC, with significant catches also being taken in the northwest Pacific and the eastern-central Pacific (the latter area covered by the SPC and the IATTC). The FAO database, however, includes reports of just 8,165 t of pelagic shark species landed from the Pacific in 2002 (Table 14.2). These self-reported figures grossly underestimate the actual pelagic shark mortality by species when compared to other fisheries analyses and landings based on trade data. For example, Bonfil (1994) estimated that 38,900 t of blue, oceanic whitetip, and silky sharks were taken from the SPC zone alone in 1989, and an additional 39,000 t of blue sharks north of the SPC zone in 1988. In 1988, the entire pelagic shark landings reported to FAO were 141 t of blue sharks and 733 t of shortfin mako sharks. Using species-specific catch rates in conjunction with fishing effort and average shark weights, Stevens (2000) estimated that a combined total of 283,100–470,400 t of pelagic sharks were taken in Pacific high-seas fisheries in 1994, including blue (140,100 t), oceanic whitetip (52,100–239,400 t), silky (84,100 t), shortfin mako (4,100 t), and thresher (2,700 t) sharks. The Oceanic Fisheries Programme (OFP) of the SPC has estimated the total catch of sharks and other nontarget species in the WCPFC statistical area for all longline and purse-seine fleets in the SPC database; however, these estimates do not include all the fleets that fish in the WCPFC area, and so may underestimate the total mortality in the region (Fig. 14.3; OFP, 2006). Estimated catches for 2002 were 57,367 t of blue, 8,650 t of silky, 7,313 t of oceanic whitetip, and 6,962 t of mako sharks. Over 99% of the pelagic shark catches were from longlines. Sharks were the second most numerous taxonomic group in the catch, following tunas, representing 25% of the catch on longliners and 7% on purse seiners.

Commercial Fisheries for Open Ocean Sharks

Blue

Makos

Oceanic whitetip

Silky

175

Other

140,000 120,000

Catch (t)

100,000 80,000 60,000 40,000 20,000

2004

2003

2002

2001

2000

1999

1998

1997

1996

1995

0

Year Fig. 14.3 Estimated catches in the Western and Central Pacific Fisheries Commission statistical area, from observer data in the SPC database (OFP, 2006).

Despite their frequency in the catch, sharks in the western-central Pacific longline fishery are generally retained at low rates. After classifying finned sharks as discards, Lawson (2001) calculated that 63% of sharks and rays recorded by OFP observers in the westerncentral Pacific longline fishery were discarded, and 71% of those animals were discarded dead. Only 13% of sharks and rays were retained (the disposition of 23% of sharks and rays was not known). Nearly 93% of sharks in the OFP observer data set were pelagic sharks. A review of observer data from Japanese vessels fishing in Australian waters during the 1980s revealed that mako, thresher, silky, and oceanic whitetip sharks were commonly retained, while blue sharks and porbeagles were finned and discarded (Bailey et al., 1996). Williams (1999) reported that purse-seine vessels in the tropical western and central Pacific retained silky shark trunks at nearly twice the rate of other sharks, including makos. In the eastern tropical Pacific, according to observer data from the IATTC, between 1993 and 2004 about 56% of purse-seine sets caught silky sharks, and 21% caught oceanic whitetip sharks; bycatch rates of these species were higher in sets made around floating objects than in sets associated with dolphins or unassociated with either dolphins or floating objects (Román-Verdesoto and Orozco-Zöller, 2005). Thus, the eastern central Pacific tuna fisheries are a significant source of mortality for pelagic sharks, although less so than the fisheries farther west. Fisheries in the northern Pacific are discussed below in the country reports for Japan and the United States.

Pelagic sharks in Indian Ocean fisheries As in the Atlantic and Pacific Oceans, pelagic sharks in the Indian Ocean are largely caught as bycatch in tuna fisheries, in which they are the predominant taxa of bycatch. Total elasmobranch catches reported to FAO from the Indian Ocean have been gradually increasing since the 1950s, and increased from 177,000 t in 1988 to 269,000 t in 2002 (FAO, 2006). These catches are fairly evenly split between the western and eastern Indian Ocean (Smale, 2008). If 60% of these landings were sharks (Bonfil, 1994), then shark

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catches have increased from 106,000 to 161,000 t. Much of this increase may be attributable to increased reporting of shark catches (Smale, 2008). In the FAO database, only 7% of the chondrichthyan catches from the Indian Ocean have been identified to species, compared with 26% from the Atlantic and 11% from the Pacific. Of the 7% identified by species, pelagic sharks comprise 55% (10,515 t). Silky sharks are the most common, followed by blue and shortfin mako sharks (Table 14.2). According to the IOTC landing statistics, the majority (83% in 2002) of shark catches in the Indian Ocean are taken by gill nets, with another 12% taken by longlines (IOTC, 2006). However, the total shark landings in the IOTC database in 2002 (79,000 t) are less than the shark landings reported to FAO for the Indian Ocean (269,000 t), implying that IOTC does not collect data from all fleets in the area. Most of the gill-net elasmobranch catches in coastal areas are of coastal rather than pelagic sharks, although blue, oceanic whitetip, shortfin mako, thresher, and silky sharks have been recorded in gill nets in the Indian Ocean. The longline fisheries report catching the same pelagic shark species, as well as porbeagle and longfin mako (IOTC, 2005a, 2006). Bonfil (1994) estimated that shark bycatches in Indian Ocean fisheries in 1989 were 75,180 t from longlines, 6,108 t from high-seas drift nets, and 1,122 t from purse seines, using an extrapolation of bycatch rates to the total effort in the region. These estimates apply to all elasmobranch species, although pelagic species would be expected to dominate the catch, at least in the high-seas gill-net and longline fisheries. Romanov (2002) extrapolated bycatch rates for purse-seine sets and estimated a total bycatch of pelagic sharks in the western Indian Ocean of 944 t in 1985, increasing to 2,068 t in 1994, a level that is broadly consistent with Bonfil’s (1994) estimate for purse seines. The IOTC has some historical data on shark catches and bycatches, but the data set is incomplete. Many countries, if they report shark catches at all, report only sharks that are retained, and do not identify sharks to species (IOTC, 2005a). However, the IOTC Working Party on Bycatch, which met for the first time in 2005, has requested IOTC member nations to report additional information on bycatch species, including sharks.

A catalog of pelagic-shark-fishing nations The following sections present brief summaries of the pelagic shark fisheries of the major elasmobranch-fishing nations, here defined as those reporting annual elasmobranch landings of over 10,000 t (Bonfil, 1994). There were 22 major shark-fishing nations in 2002, with Indonesia, India, Spain, Pakistan, and Taiwan reporting the highest elasmobranch landings (Table 14.3), which accounted for 42% of the global landings in that year. Information on catch composition, discards, and offshore and distant-water fleets taking pelagic sharks varies widely among nations, and so the following qualitative assessments should be considered preliminary. Because it is currently impossible to determine the actual size of their pelagic shark landings, these countries are presented alphabetically in two subjective groups: Major and moderate pelagic-shark-fishing nations based on a review of factors, including their fin exports to Hong Kong, their distant-water fleets, and their fisheries taking pelagic sharks (Table 14.3). Bonfil (1994), Vannuccini (1999), and Fowler et al. (2005) provided detailed summaries of the historical fluctuations in these elasmobranch fisheries, but are not specific to pelagic elasmobranchs. Chen (1999) provided details about the domestic and international markets for shark products (Table 14.4).

Table 14.4 Commercially important pelagic shark species by country and use.a Country

White

Oceanic whitetip

M (d) M (d); F (e)

M (d); F (e); sport

M (d, e)

Makos

Porbeagle

Silky

Threshers

Unidentified

M (d); F (e) M (e, i); F (e, i)

M (d, e)

M (d, e) M (d, e, i); F (d, i, re-ex)

M (d); F (e) M (d) M (d); F (e) M (d, e) M (d, i)

M (e) M (d); F (e) M (d, e) M (d, i, re-ex)

M (d, i, re-ex); F (d, e)

F (i) M (i, e); F (i)

M (d); F (e) M (d); F (e) M (e); sport M (d) M (d); F (e)

M (d) M (d) M (d); F (e)

M (d); F (e)

M (d, e) M (d, i, re-ex)

M (d) M (d, i)

M (d); F (e) M (d); F (e)

M (d) F (e)

M (d); F (e) M (d); F (e)

M (d, e); F (e) F (d)

F (i) M (i); F (i) M (e, i) M (d); F (e) M (d, e, i) M (e, i); F (e, i) M (e) M (d, i, re-ex); F (i)

M (e) M (d) (Continued)

Commercial Fisheries for Open Ocean Sharks

Argentina Australia Bangladesh Belgium Brazil Canada China (Hong Kong) Cuba Cyprus Fiji France Germany Greece India Indonesia Ireland Italy Japanb Kenya Korea, Republic of Malaysia Maldives Mexico Mozambique The Netherlands New Zealand

Blue

177

178

Country Nigeria Norway Pakistan Peru Philippines Portugal Seychelles Singapore Solomon Islands South Africa Spain Sri Lanka Taiwan Tanzania Thailand Turkey United Kingdom United States Uruguay a

Blue

White

Makos

Oceanic whitetip

Porbeagle

Silky

Threshers

Unidentified

F (e) F (e) M (d); F (e)

M (d); F (e) M (d)

M (d); F (e)

M (d, i); F (e, i) M (d); F (e)

M (d); F (e)

M (d); F (e)

M (d); F (e) M (d); F (e) M (d); F (d)

M (d); F (e) M (d, e) F (d, i, e) M (d); F (e) M (e, i); F (e, i) M (e, i) M (e, i); F (e, i)

M (d); F (e) F (e, i) M (d); F (e) M (d, e) M (d, e); F (e)

M (d); F (e) M (d, i) M (d)

M (d)

M (d, e) M (d, i)

F (i) M (d, i)

Major shark-fishing nations are italicized. Brazil, Nigeria, Peru, and Portugal were not included in Chen (1999) but were major shark-fishing nations in 2002. M: meat; F: fins; d: domestic consumption; e: exports; i: imports; re-ex: re-exported; Chen (1999). b Also, salmon shark: M (d, heart); F (e).

Sharks of the Open Ocean

Table 14.4 (Continued).

Commercial Fisheries for Open Ocean Sharks

179

Major pelagic-shark-fishing nations Brazil’s elasmobranch landings have exceeded 10,000 t annually since 1966 (FAO, 2003a). Three different tuna and swordfish longline fleets in Brazil take sharks as bycatch. Blue, silky, and oceanic whitetip sharks, along with other Carcharhinus species, are taken in the Natal longline fishery in the northeast. These species, plus shortfin mako and thresher sharks, are also taken in the Santos longline fishery off the southeast coast (Amorim et al., 1998). In 2004, Brazil reported about 5,000 t of pelagic sharks taken by about 120 tuna longline vessels in the South Atlantic (ICCAT, 2005; Hazin et al., 2008), which is about one-fourth of Brazil’s reported elasmobranch landings. At least eight pelagic shark species are taken in this region, of which 60% are blue sharks. Since the late 1970s, as markets for meat and prices paid for fins increased, shark landings have grown, as has the tendency to sometimes target blue sharks (Amorim et al., 1998). Indonesia is the world’s most important elasmobranch-fishing nation, with the highest sustained rate of fishery growth (Bonfil, 1994). Reporting 106,000 t in 2002, it accounts for 13% of global elasmobranch landings (FAO, 2003a, 2006). Indonesia also has the richest chondrichthyan fauna in the world, with an estimated 350 species (P. Last, personal communication, as cited in Keong, 1996). Since the late 1980s, Indonesian shark fisheries have been driven by the demand for fins (Suzuki, 2002). Landings are not species specific, but are reported at the level of “sharks” and “rays.” Although sharks still dominate the landings, the proportion dropped from 66% through the early 1990s (Bonfil, 1994) to 55% in 1997 (SEAFDEC, 2001). Most elasmobranchs are caught opportunistically throughout Indonesian waters, mainly in coastal artisanal fisheries and as bycatch by commercial shrimp trawlers (Keong, 1996). A few domestic fisheries targeting sharks have resulted in localized depletions, but because they operate in coastal waters they have not involved pelagic species. However, an increasing number of foreign longline vessels (from Taiwan and Korea with Indonesian crew) are targeting sharks in Indonesian waters, taking mainly blue sharks. It was estimated that this fishery alone, based in Bitung, North Sulawesi, probably caught at least 12,900 t of blue sharks in 1993, or more than 20% of Indonesia’s shark catch in that year (Keong, 1996). Japan may have the longest history of commercial shark fishing – it has been exporting shark fins to China for more than 200 years (Nakano, 1999). Japan led in world elasmobranch landings from the 1950s to the early 1970s (103,000 t in 1954), but annual landings fell to less than 33,000 t in 2002 (FAO, 2003a, 2006). The three Japanese fisheries that take pelagic sharks are all tuna longline fisheries: A coastal fleet operating near Japan, an offshore fleet in the northwestern Pacific, and a distant-water fleet in all three oceans (Nakano, 1999). Pelagic sharks are mostly taken as bycatch in these fisheries (usually 10% of total catch); however, a longline fishery off northern Japan targets salmon sharks (Simpfendorfer et al., 2005). In the 1990s, the major pelagic sharks caught in Japan’s tuna longline fisheries were blue shark (75% of shark bycatch), bigeye thresher (15%), oceanic whitetip (4%), silky (2%), and shortfin mako (1%). Distant-water fleets usually retain only mako sharks and fins from all species. In the North Pacific, blue shark is also the dominant elasmobranch taken in the salmon gill-net fishery (63% of elasmobranch bycatch), the flying squid drift-net fishery (93%), and the large-mesh drift-net fishery (84%; Nakano, 1999). Salmon sharks are also caught incidentally in coastal fisheries. In the Atlantic, Japan’s tuna fleet is now required to

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Sharks of the Open Ocean

submit logbooks reporting shark bycatch by species (ICCAT, 2005). Overall, blue sharks represent 61–79% of the Japanese tuna fleet’s bycatch, followed by salmon (10%), shortfin mako (10%), and thresher sharks (5%; Matsunaga et al., 2003). Mexico has led North American elasmobranch landings nearly every year since 1950, with more than 10,000 t recorded annually since 1973 (FAO, 2003a). By the 1990s, the prices paid for fins were a major driver in Mexican shark fisheries, and many pelagic sharks are currently finned and discarded (Sosa-Nishizaki et al., 2008), with fins exported to the United States for re-export to Asia (Rose, 1998). Landings are not reported by species but are classified according to size: Large sharks measuring more than 150 cm are labeled “tiburon,” and small sharks less than 150 cm are “cazon,” which can include juveniles of larger species. Shark fishing occurs in all coastal Mexican states, and about onethird of reported elasmobranch landings are from Gulf of Mexico and Caribbean waters, and are primarily composed of coastal species (Bonfil, 1997). The remainder of the landings are from the Pacific and Gulf of California (SAGARPA, 2000; FAO, 2003a). Virtually all of the fisheries that catch sharks are multispecies, seasonal, and largely artisanal: 80% of catches in the Gulf of Mexico are taken by small boats (10 m) fishing within 20 nautical miles of shore (Rose, 1998). In Mexico’s Pacific fisheries, six shark species are known to be of commercial importance: Common thresher, blue, angel (Squatina californica), shortfin mako, spiny dogfish (Squalus acanthias), and school (Galeorhinus galeus) sharks. Two major fisheries target sharks within the exclusive economic zone (EEZ) off the Pacific Coast, where fishers land and use virtually every size and species of shark caught: An artisanal, small-boat fleet (possibly 2,000 vessels) that targets sharks close to shore and an offshore drift-net fishery for swordfish and sharks that began in 1986 (Holts et al., 1998). In addition, a longline fleet (up to 21 vessels) targeting tunas and billfishes began operating within the EEZ in 1980, and up to 25% of their catch was pelagic sharks. In 2007, there were six permitted large-scale (20 m) longline vessels that target sharks off Mexico’s Pacific Coast (L. Castillo, personal communication). Pakistan has been a world leader in elasmobranch fishing since the 1960s, landing nearly 50,000 t in 2002 (FAO, 2003b), yet little is known of its shark fishery (Bonfil, 1994; Anderson and Simpfendorfer, 2005). Landings largely consist of carcharhinid sharks, taken mainly by gill nets. In general, marine fishing is confined to intensive exploitation of inshore resources (FAO, 2003b). However, Bonfil (1994) described a pelagic gill-net fleet that operates in waters as far away as Somalia; although the catch composition is not known, the fleet likely takes large numbers of pelagic sharks. The development and expansion of high-seas tuna longlining and other fisheries offshore is under way (FAO, 2003b). Republic of Korea has been a major elasmobranch-fishing nation since at least 1968, with reported landings averaging 18,000 t (FAO, 2003a). In general, landings are recorded by gear type, with virtually none recorded by species (Bonfil, 1994); the fisheries taking pelagic sharks are not well described. South Korea supports directed shark fisheries with gill nets in both adjacent and distant waters (Rose, 1996). Thresher, mako, salmon, blue, and white sharks are among the main species taken in the adjacent-water directed fisheries (Parry-Jones, 1996). A marked decline in shark landings from these fisheries over the past 30 years suggests a declining trend in shark populations, rather than a shift of market forces or fishing effort. Although its distant-water fleets operate in all oceans, the majority of the shark landings come from bycatch in Pacific-based fisheries (Parry-Jones, 1996).

Commercial Fisheries for Open Ocean Sharks

181

South Korea initiated an observer sampling program in 2002; in 2005, observers on longliners found that 21% (by number) of the bycatch in the western and central Pacific and 19% in the eastern Pacific were pelagic sharks (An et al., 2006). Spain is one of the most important elasmobranch-fishing nations, having ranked among the top five since 1997, with over 60,000 t in 2002 (Table 14.3; FAO, 2003a). It is also among the top three exporters of shark fins to the Hong Kong fin market (Table 14.3; Clarke and Mosqueira, 2002; Anonymous, 2006). Spanish longline vessels take sharks largely as bycatch in the Mediterranean and in the Atlantic and Indian Oceans, but some targeting of pelagic sharks also occurs. For example, the Spanish fleet in the Mediterranean moves into deeper water in the summer to target pelagic sharks (especially shortfin mako, blue, and thresher sharks) along with swordfish, and a small longline fleet targets blue sharks in the Bay of Biscay (SGRST, 2002, in Walker et al., 2005). Blue shark and shortfin mako compose the majority of the landings from the Atlantic longline and gill-net fleets, with blue sharks accounting for 60–70% of Spain’s total shark catch (Fleming and Papageorgiou, 1996). Little is known about the size of Spain’s shark catches, discards, or species composition from the distant-water fleets before the mid-1990s (Rose, 1996), when Spain began reporting shark catches based on observer data (FAO, 2003a). Between 1995 and 2002, Spain’s Indian Ocean landings, which likely consist mainly of pelagic sharks, steadily increased and topped 16,000 t in 2002, or 25% of Spain’s elasmobranch landings. About 80% of the marine fish catch in Sri Lanka consists of pelagic fishes, with sharks second only to tunas in number (Joseph, 1999). Although the elasmobranch catch composition is poorly documented (Bonfil, 1994), all three threshers, both makos, and silky, oceanic whitetip, and blue sharks are taken incidentally in drift gill-net and bottom longline fisheries (Joseph, 1999). Silky sharks may account for more than 50% of the shark landings by weight; the oceanic whitetip, pelagic thresher, and shortfin mako are also important. A drift longline fishery targeting pelagic sharks developed in the 1980s, driven largely by the export market for fins. Despite increased fishing effort offshore (in the EEZ and beyond) during the late 1980s and mid-1990s, shark landings and catch per unit effort (CPUE) declined, calling into question the sustainability of these pelagic shark resources (Joseph, 1999). Reported silky shark landings fell steadily from 9,760 t in 2000 to 2,340 t in 2005 (Sri Lanka Ministry of Fisheries and Aquatic Resources Development, 2006). Taiwan has been taking large numbers of sharks since the 1930s. Chen et al. (1996, 2002) provided a detailed discussion of Taiwan’s shark fisheries, which target pelagic sharks in coastal, offshore (out to 200 miles), and distant waters, and take them as bycatch in all oceans (Rose, 1996). About 14% of Taiwan’s shark landings come from its offshore fisheries (Chen et al., 1996), and another 85% is caught by its distant-water tuna fleet, which operates widely in the Pacific, Atlantic, and Indian Oceans, although the three primary shark-fishing grounds are in the EEZs of Papua New Guinea, Mozambique, and Indonesia (Chen et al., 2002). Since at least the early 1990s, Taiwanese longline vessels have been targeting sharks in Indonesian waters and are responsible for a large proportion of the pelagic shark landings (largely silky sharks) reported from Indonesia (Keong, 1996; Rose, 1996). Pelagic sharks make up between 48% and 78% of the sharks being sold at two of Taiwan’s harbors, which together account for 85% of Taiwan’s coastal and offshore shark landings (Chen et al., 2002). Although official Taiwanese statistics provide no species information, silky, oceanic whitetip, shortfin mako, thresher, hammerhead (Sphyrna spp.),

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Sharks of the Open Ocean

and blue sharks are common in Taiwan’s distant-water catches, while bigeye and pelagic threshers, hammerheads, sandbar (Carcharhinus plumbeus), oceanic whitetip, silky, dusky (C. obscurus), spinner (C. brevipinna), blue, and shortfin mako sharks are caught in the coastal and offshore fisheries (Chen et al., 2002). Apparently, only blue sharks are finned at sea, with other species more fully utilized. Pelagic fisheries of the United States operate off the Atlantic, Gulf of Mexico, and Pacific Coasts and in the central Pacific (see regional summaries in Fowler et al., 2005). Total elasmobranch landings in 2002 were 24,076 t (FAO, 2003a). With the exception of a small directed porbeagle fishery in the Atlantic and a gill-net fishery landing modest numbers of thresher and mako sharks in the Pacific, pelagic sharks are taken almost exclusively as bycatch in US commercial fisheries. In general, US elasmobranch fisheries are well described, with mandatory species-specific reporting of landings and discards and catch limits placed on some species. In the Atlantic, 120 active longline vessels target tunas and swordfish, with shortfin mako, thresher, and porbeagle sharks as secondary targets and blue sharks discarded as bycatch. Pelagic shark commercial landings from the Atlantic (dominated by mako sharks) steadily increased through the 1990s, peaking in 1996 at 676 t (National Marine Fisheries Service, NMFS, 2004). In that same year, dead discards totaled 949 t in the longline fishery (NMFS, 2004) and 110 t in other fisheries (NMFS, 2001). Off the Pacific Coast, common threshers are targeted in a drift gill-net fishery (landings of 200–400 t/year since 1994) that also lands smaller numbers of other thresher species and shortfin makos; blue shark discards in this fishery exceed the target catch (PFMC, 2003). In the North Pacific, salmon sharks are not targeted yet account for 12% of the shark bycatch in the massive Alaskan groundfish fisheries (NMFS, 2001). The Hawaii-based longline fleet (110 vessels in 2003) targets tunas and swordfish, but sharks are the dominant species caught (by number) on swordfish trips (Ito and Machado, 1997). In 1991, most sharks were released alive, but by 1998 at least 61% of the shark catch, 90% of which were blue sharks, was finned (Camhi, 1999). Reported shark catches and finning have declined with the implementation of anti-finning laws in both Hawaii (2000) and at the federal level (2002). The United States was the second largest exporter of shark fins to Hong Kong in 1999 with 565 t (Table 14.3; Clarke and Mosqueira, 2002); most of these fins, however, originated outside US waters and fisheries. Since 2001, the United States has dropped out of the top 10 fin exporters to Hong Kong (Anonymous, 2006).

Moderate pelagic-shark-fishing nations The following shark-fishing nations either land fewer pelagic elasmobranchs than the nations discussed in the preceding section or too little is known of the species composition of their shark fisheries to determine the relative size of their pelagic shark catches. Nonetheless, even a relatively low proportion of pelagic sharks in the overall elasmobranch catch can result in significant pelagic shark mortality year after year for countries reporting sizable elasmobranch landings (e.g., India). These countries are reported alphabetically. Argentina has led South America in elasmobranch landings since 1993 (FAO, 2003a), and reported over 26,000 t in 2002. Although a few sharks (e.g., Galeorhinus galeus) and rays are targeted, pelagic species (e.g., porbeagle and shortfin mako) taken as bycatch in

Commercial Fisheries for Open Ocean Sharks

183

longline fisheries contribute little to total elasmobranch landings (Chiaramonte, 1998; Caro Ros, 1999). Canada has sizable shark-fishing operations in the Atlantic, including the directed fishery for porbeagle sharks that began in 1961 (Campana et al., 2008). Porbeagle landings by all nations off the Atlantic Coast of Canada peaked at 9,281 t in 1964, but subsequently declined to less than 600 t by the late 1970s (Campana et al., 2002). Pelagic sharks in Canadian waters have been under management since 1995, and to halt overfishing in the porbeagle fishery, an annual quota of 200 t was established for the period 2002–2007 (DFO, 2002). Canada also supports a small directed blue shark fishery in the Atlantic that has a 250 t annual quota, but since 1986 reported blue shark catch and bycatch has averaged about 1,000 t/year (Campana et al., 2005). However, the total blue shark catch in the Canadian Atlantic by both domestic and foreign longline fisheries may actually be 20 times larger. Shortfin makos and other sharks are taken as bycatch in various longline fisheries but are not subject to catch limits. Pelagic sharks are not targeted off Canada’s Pacific Coast. Prior to the 1990s, France led European countries in elasmobranch landings (Fleming and Papageorgiou, 1996) and reported just over 23,000 t in 2002 (FAO, 2003a). French vessels fish in the Atlantic and Indian Oceans and in the Mediterranean Sea. The vast majority of elasmobranch landings are taken as bycatch and are benthic and coastal species. However, a targeted fishery for porbeagles in the Atlantic reported taking 461 t in 2002, or about 2% of France’s total elasmobranch landings (FAO, 2003a). India has been among the top five elasmobranch-fishing nations since the 1970s, with landings of almost 67,000 t in 2002 (FAO, 2003b), but the species composition of the catch is not reported. Sharks compose 55–70% of its elasmobranch landings (Hanfee, 1999; Vannuccini, 1999). They are taken mainly as bycatch from coastal Indian Ocean waters off both coasts (FAO, 2003a). Although there is no organized industrial fishery for pelagic sharks, tuna longliners are known to take blue sharks, threshers, and shortfin makos (Hanfee, 1999), but the size of this bycatch is not known. Although India is a major exporter of fins to Hong Kong, pelagic sharks are not important among these fin exports (Anderson and Simpfendorfer, 2005). The government supports the expansion of India’s shark fisheries, and increased mechanization in the future will allow fishing farther from shore. For Malaysia, which does not have a distant-water fleet, virtually all elasmobranch landings are taken in the east Indian and west-central Pacific Oceans (Keong, 1996), largely as bycatch in demersal trawl fisheries (Bonfil, 1994; Ali et al., 1999). There is little information on the species composition of the elasmobranch catch; however, it is estimated that batoids account for 60–80% of the catch (Bonfil, 1994; Ahmad, 2002). A study by TRAFFIC International does not highlight any pelagic sharks in the landings (Keong, 1996). Although there are some indications that elasmobranchs in Malaysian waters are at least fully exploited (Ahmad, 2002), there are currently no fishery management measures for sharks or rays (Keong, 1996). In the Maldives, at least seven pelagic sharks are caught, including shortfin mako, silky, oceanic whitetip, blue, and all three species of threshers (Anderson and Hafiz, 2002). They are targeted in the longline fishery (in which silky sharks account for up to 80% of the catch by numbers) for their fins and meat, and are taken as bycatch in the pole-and-line tuna fishery and by handline. Two other directed shark fisheries target reef sharks and deep demersal sharks; all are driven by export demand for fins and dried meat.

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The offshore longline fishery has expanded in recent years (Anderson and Simpfendorfer, 2005). However, most Maldivian tuna fishermen are strongly opposed to pelagic longlining for sharks: They believe that tuna follow silky sharks, and that if the sharks are removed, then the tuna will disperse (Anderson and Hafiz, 2002). Despite these conflicts and concerns over the sustainability of the oceanic shark fishery, no management measures are in place. New Zealand’s elasmobranch fisheries, both targeted and incidental, are well documented by commercial fishing and observer data, and elasmobranch landings between 1993 and 2002 averaged 17,597 t (FAO, 2003a). There are three directed fisheries for elasmobranchs, but pelagic sharks are not targeted, nor are they among the top six commercially important elasmobranch species (Francis and Shallard, 1998). However, the blue shark is the most common species caught (by number) in New Zealand’s tuna longline fisheries, with porbeagle and mako sharks (combined) ranked fifth (Francis et al., 1999). Other pelagic elasmobranchs caught incidentally include (in order of importance) pelagic stingray, common thresher, bigeye thresher, oceanic whitetip, and white sharks. In 1997–1998, 45,000 blue sharks (1,400 t), 4,000 porbeagles (150 t), and 3,000 makos (200 t) were caught on tuna longlines. Most of these sharks were immature and alive when recovered (Francis et al., 2001). The vast majority of blue sharks are finned and discarded, as are porbeagles, while makos are retained more often for their fins and meat. The recreational angling community has expressed concern that surface longlining is depleting makos in New Zealand waters, and has called for a domestic ban on shark finning. Nigeria is the only major elasmobranch-fishing nation in Africa. Since 1967, reported elasmobranch landings have exceeded those of all other African nations, with annual landings of over 13,000 t since 1998 (FAO, 2003a). Yet relatively little is known of Nigeria’s elasmobranch fisheries. There are no large-scale commercial longline or purse-seine fleets fishing legally in Nigerian waters, but shark finning by foreign vessels fishing illegally has been reported. A small-scale artisanal fleet targets sharks with drift nets, and sharks are taken as bycatch in the shrimp trawl fishery (Walker et al., 2005). As neither Rose (1996) nor Vannuccini (1999) discuss Nigeria in their reports on elasmobranch trade, it is possible that Nigeria does not report its shark exports or that its elasmobranch resources (other than fins) are consumed domestically. There is no information on the species composition of the catch. Peru was a major elasmobranch-fishing nation in the 1960s through the 1980s; landings fell below 10,000 t in the 1990s, but subsequently increased to 16,633 t in 2002 (FAO, 2003a, 2006). Yet sharks are of negligible importance relative to other Peruvian fisheries resources (Bonfil, 1994; Caro Ros, 1999). Although the majority of the reported landings are Mustelus spp. (Bonfil et al., 2005), pelagic sharks taken as bycatch on longlines targeting tuna include blue sharks (the most common species caught), shortfin makos, threshers, oceanic whitetips, silky sharks, and pelagic stingrays (Cook, 1995; Caro Ros, 1999). Portugal recorded 14,016 t of elasmobranch landings in 2002, but since 1990, landings have fluctuated between 8,386 t (1998) and 30,495 t (1991) (FAO, 2003a). Portuguese landings have been reported to FAO from the Atlantic since at least 1950, and from the Indian Ocean since 1999. Despite recent efforts to describe Portugal’s elasmobranch fisheries, there is limited information on the fisheries catching pelagic sharks, although blue sharks are thought to be heavily targeted (Correia and Smith, 2003). Shortfin mako,

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common thresher, and porbeagle are also taken in the targeted surface longline fishery and as bycatch in gill-net, purse-seine, and bottom trawl fisheries targeting teleosts (Correia and Smith, 2003). Blue and shortfin mako sharks are taken as bycatch in the Portuguese swordfish longline fleet operating in the Azores, where blue sharks may represent up to 86% of total landings (Aires-da-Silva et al., 2008). Blue shark catch rates steadily increased between 1993 and 1998, suggesting that this Azores-based fishery may shift effort to target blue sharks, which were previously discarded but are now retained, on a seasonal basis when swordfish are less available. Thailand reported nearly 22,000 t of elasmobranch landings in 2002 (FAO, 2003a), with shark fins the main target for shark fisheries (Vidthayanon, 2002). There are no directed fisheries for pelagic elasmobranchs, but the fins and meat are used from virtually all sharks taken in the bycatch of the trawl and gill-net fisheries. All three species of threshers, both species of makos, and oceanic whitetip, blue, and silky sharks are found in Thailand’s waters, but its elasmobranch landings are dominated by batoids (Vidthayanon, 2002). Depletion from overfishing in Thailand waters (for all species) has forced Thai fleets into international waters as far away as the South China Sea (Keong, 1996; Vidthayanon, 2002). The large elasmobranch landings from the United Kingdom are primarily from the targeted and incidental take of piked (or spiny) dogfish (Squalus acanthias) and batoids (Pawson and Vince, 1999), which accounted for 63% and 36%, respectively, of the total elasmobranch landings during the 1970s and 1980s (Bonfil, 1994). Blue sharks and porbeagles are targeted in coastal waters off Cornwall (Fleming and Papageorgiou, 1996; Pawson and Vince, 1999), and are taken as bycatch with threshers and shortfin mako in the high-seas fisheries targeting tunas and billfish (Fowler et al., 2004). UK porbeagle landings remain negligible (Vannuccini, 1999).

Discussion Global reported catches of elasmobranchs have increased over the last 50 years, particularly in the Indian Ocean. Overall, only 15% of these catches have been identified at the species level. Thus, an accurate, quantitative evaluation of the total number of pelagic elasmobranchs killed by fisheries each year remains elusive. It was impossible to accurately determine total pelagic shark landings, the relative importance of pelagic sharks in the overall elasmobranch catch, or the catch composition of the shark fisheries as a whole and for pelagic sharks, either by ocean basin or by country, for most of the 22 major elasmobranch-fishing nations. Canada, Japan, New Zealand, and the United States provide the most complete picture of shark bycatch in their longline and net fisheries, in large part because they require the species-specific reporting of catches and support at-sea observer and research programs. The number of countries reporting species-specific catch data to the RFMOs and the FAO has increased over the last decade, in response to requests for better bycatch data by RFMOs such as ICCAT, IOTC, and WCPFC. However, the fraction of catches identified to species remains low, and many major shark-fishing nations have not improved their catch reporting. Where species-specific data are available, the vast majority of the pelagic shark catches are blue sharks, followed by silky and mako sharks.

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On the basis of the foregoing assessment, the top five pelagic-shark-fishing nations are believed to be Indonesia, Japan, Spain, Sri Lanka, and Taiwan, while Brazil, Mexico, Pakistan, Republic of Korea, and the United States are also important pelagic shark fishers. Another 12 countries – Argentina, Canada, France, India, Malaysia, the Maldives, New Zealand, Nigeria, Peru, Portugal, Thailand, and the United Kingdom – are moderate contributors to global pelagic elasmobranch catches because their shark landings are mainly from coastal fisheries and consist largely of coastal sharks and/or batoids. This review evaluated only countries reporting more than 10,000 t of elasmobranchs to FAO in 2002, but it is likely, given gaps in the catch data reported to FAO, that other fishing nations may also contribute significantly to the catch of pelagic elasmobranchs. Many countries have fisheries that target pelagic sharks. However, the vast majority of pelagic elasmobranchs are probably taken as bycatch on longlines and nets targeting other species, especially tunas and swordfish in international waters. China, Japan, Republic of Korea, Spain, and Taiwan currently support the largest distant-water fleets, which fish outside their own EEZs throughout the Atlantic, Pacific, and Indian Oceans (Phipps, 1996; Bonfil et al., 1998). For example, in Indonesia, pelagic shark landings soared in the mid1980s with the introduction of Taiwanese longliners (Keong, 1996). Expanding global markets for shark products and the growth of high-seas fisheries have intensified fishing pressure on open ocean sharks. This fisheries expansion has taken place in the absence of comprehensive data collection programs and sound fishery management regimes. Nascent efforts to evaluate the impact of high-seas fisheries on pelagic sharks should be expanded through the commitment of scientific and management resources by fishing countries and regional fisheries management organizations, as recommended by FAO in the IPOA for Sharks (FAO, 1999), CITES, and IUCN (Cavanagh et al., 2008). All of the pelagic sharks examined in this chapter have been recognized as biologically vulnerable to depletion. While some data collection and management regimes are being developed and implemented, regional fisheries management organizations should take immediate steps to improve species-specific catch data on oceanic sharks and to evaluate the sustainability of those catches.

Acknowledgments The authors thank The David and Lucile Packard Foundation for support of the Marine Program of the Wildlife Conservation Society, and the Pew Charitable Trusts for support of the Pew Institute for Ocean Science. Shelley Clarke, Rachel Cavanagh, Tim Lawson, Sonja Fordham, and John Stevens provided helpful suggestions.

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Phipps, M. J. (1996) TRAFFIC report on shark fisheries and trade in the East Asia region. In: World Trade in Sharks: A Compendium of TRAFFIC’s Regional Studies, Vol. I. TRAFFIC International, Cambridge, UK, pp. 7–19. Román-Verdesoto, M. and Orozco-Zöller, M. (2005) Bycatches of Sharks in the Tuna Purse-Seine Fishery of the Eastern Pacific Ocean Reported by Observers of the Inter-American Tropical Tuna Commission, 1993–2004. Data Report 11. IATTC, La Jolla, CA. Romanov, E. V. (2002) Bycatch in the tuna purse-seine fisheries of the western Indian Ocean. Fishery Bulletin 100(1), 90–105. Rose, D. (1996) An Overview of World Trade in Sharks and Other Cartilaginous Fishes. TRAFFIC International, Cambridge, UK, 106 pp. Rose, D. (1998) Shark Fisheries and Trade in the Americas. Vol. 1. North America. TRAFFIC North America, Washington, DC, 201 pp. SAGARPA (Secretaría de Agricultura, Ganadería, Dessarollo Rural, Pesca y Alimenacíon) (2000) Anuario Estadístico de Pesca 2000. www.conapesca.sagarpa.gob.mx/wb/cona/cona_anuario_ estadistico_de_pesca, accessed 22 December 2006. SEAFDEC (Southeast Asian Fisheries Development Center) (2001) Fishery Statistical Bulletin for the South China Sea Area. Bangkok, Thailand, 155 pp. Shotton, R. (ed.) (1999) Case Studies of the Management of Elasmobranch Fisheries. FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, 479 pp. Simpfendorfer, C. A., Cavanagh, R. D., Tanaka, S. and Ishihara, H. (2005) Northwest Pacific regional overview. In: Sharks, Rays and Chimaeras: The Status of the Chondrichthyan Fishes (eds. S. L. Fowler et al.). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 150–161. Smale, M. J. (2008) Pelagic shark fisheries in the Indian Ocean. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Sosa-Nishizaki, O., Márquez-Farías, J. F. and Villavicencio-Garayzar, C. J. (2008) Case study: Pelagic shark fisheries along the west coast of Mexico. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Sri Lanka Ministry of Fisheries and Aquatic Resources Development (2006) Table 2: Capture fish production by major species. www.statistics.gov.lk/agriculture/fishery/, accessed 21 December 2006. Stevens, J. D. (2000) The population status of highly migratory oceanic sharks. In: Getting Ahead of the Curve: Conserving the Pacific Ocean’s Tunas, Swordfish, Billfishes and Sharks (ed. K. Hinman). National Coalition for Marine Conservation, Leesburg, VA. Suzuki, T. (2002) Development of shark fisheries and shark fin export in Indonesia: Case study of Karangsong Village, Indramayu, West Java. In: Elasmobranch Biodiversity, Conservation and Management (eds. S. L. Fowler, T. M. Reed and F. A. Dipper). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 149–157. Vannuccini, S. (1999) Shark Utilization, Marketing and Trade. FAO Fisheries Technical Paper No. 389. FAO, Rome, Italy, 470 pp. Vidthayanon, C. (2002) Elasmobranch diversity and status in Thailand. In: Elasmobranch Biodiversity, Conservation and Management (eds. S. L. Fowler, T. M. Reed and F. A. Dipper). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 104–113. Walker, P., Cavanagh, R. D., Ducrocq, M. and Fowler, S. L. (2005) Northeast Atlantic (including Mediterranean and Black Sea) regional overview. In: Sharks, Rays and Chimaeras: The Status of the Chondrichthyan Fishes (eds. S. L. Fowler et al.). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 71–95.

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Watson, R. and Pauly, D. (2001) Systematic distortions in world fisheries catch trends. Nature 414, 534–536. WCPFC (2006) Review Conference on the Agreement for the Implementation of the Provisions of the United Nations Convention on the Law of the Sea of 10 December 1982 relating to the Conservation and Management of Straddling Fish Stocks and Highly Migratory Fish Stocks. www.un.org/depts/los/convention_agreements/reviewconf/wcpfc_reviewconference.pdf, accessed 29 January 2007. Williams, P. G. (1999) Shark and related species catch in tuna fisheries of the tropical Western and Central Pacific Ocean. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/2. FAO, Rome, Italy, pp. 860–879.

Chapter 15

Recreational Fishing for Pelagic Sharks Worldwide Elizabeth A. Babcock

Abstract While government fisheries agencies have not documented the recreational fisheries for pelagic sharks in most countries, information exists in the records of fishing clubs, cooperative tagging programs, and the International Game Fish Association. Countries with significant pelagic shark recreational fisheries include Australia, New Zealand, the United States, and the United Kingdom. Some recreational pelagic shark fishing also occurs in Ireland, Italy, the Azores, Mauritius, South Africa, the Caribbean, and Mexico. Most pelagic shark game fishing is now catch-and-release, and the total mortality caused by recreational fisheries has been declining since the 1980s. The most commonly caught pelagic sharks are blue (Prionace glauca), shortfin mako (Isurus oxyrinchus), porbeagle (Lamna nasus), and thresher sharks (Alopias spp.). Key words: angling, game fishing, recreational fishing, Prionace glauca, Isurus oxyrinchus, Lamna nasus, Alopias.

Introduction Big-game pelagic sharks are caught by anglers who enjoy the thrill of catching a large fish and have the means to fish offshore, in either privately owned or chartered boats. The most desirable big-game shark is the shortfin mako (Isurus oxyrinchus, Lamnidae), which is known for its fighting and jumping ability, as well as being considered the best eating of the pelagic sharks (Bauer, 1991). The writer Zane Grey, who pioneered game fishing in New Zealand, called mako sharks “New Zealand’s premier sporting fish, as game as he [is] beautiful, as ferocious as he [is] enduring” (Grey, 1976). Porbeagles (Lamna nasus, Lamnidae), salmon sharks (L. ditropis, Lamnidae), and the thresher sharks (Alopias spp., Alopiidae), particularly the common thresher (A. vulpinus), are also popular because of their fighting ability (Bauer, 1991; Schultz, 2000). However, the most commonly caught pelagic shark is the blue shark (Prionace glauca, Carcharhinidae), which, although it is not known for being especially exciting either to catch or to eat, is encountered throughout the world’s oceans. This paper focuses on angling for pelagic sharks; bluewater spearfishermen Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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take sharks on occasion (e.g., International Underwater Spearfishing Association, 2005), but that fishery is small compared to angling. White sharks (Carcharodon carcharias, Lamnidae) are not considered in this review because, although they are found in open ocean waters, sport fisheries for white sharks are generally coastal.

Information sources Because pelagic sharks are often caught by anglers who are interested in size records, rather than for food or sport, the game fish records provide information about the distribution of pelagic shark recreational fishing. The International Game Fish Association (IGFA) maintains records for the largest fish ever caught of each species, and the largest fish caught with various test weights of line, with separate categories for male and female anglers. There is also special recognition for high ratios between the weight of the fish and the test weight of the line, and the largest fish caught in an annual fishing contest. In 2000, there were a total of 236 records for pelagic sharks, mainly mako (presumably mostly shortfin), blue, and thresher sharks (IGFA, 2000). Each IGFA record includes a location, which is either the port where the angler landed the fish or a landmark near the catch site (IGFA, 2000). The latitude and longitude of these locations were found in the Getty Thesaurus of Geographic Names (2005), the New Zealand Geographic Placenames Database (2005), the US Geological Survey’s Geographic Names Information System (2005), and the Geoscience Australia database (2005). They were then mapped using ArcMap 9.0 GIS software (ESRI, Inc., Redlands, California). IGFA records from 2000 were used because this was the last year in which tournament results were reported. The locations of records in 2003 were similar (IGFA, 2003).

Recreational fishing by country There were no IGFA records in 2000 from Asia or South America, and only four from Africa (all in South Africa). Ninety-one percent of the records were from just four countries: Australia (31%), the United States (28%), New Zealand (25%), and the United Kingdom (8%) (Fig. 15.1). The species caught varied widely by region (Fig. 15.2). Most of the 88 records for mako sharks were from Australia, New Zealand, and the United States, but there were also records in the Caribbean and the Indian Ocean (IGFA, 2000). Most of the 79 records for blue sharks were from Australia, New Zealand, and the US Atlantic. The 44 thresher shark records were widely distributed, including several in Italy, South Africa, the United Kingdom, and the US Pacific, as well as Australia, New Zealand, and the US Atlantic. The 21 record porbeagles were all from the United Kingdom, except for three from New Zealand and one from the United States.

Australia While sportfishing is popular throughout Australia, big-game fishing is most prevalent on the east coast. Sharks are mainly caught off New South Wales in the vicinity of Sydney,

Recreational Fishing for Pelagic Sharks

Fig. 15.1 Locations of the 236 IGFA records for the year 2000 (IGFA, 2000). The size of the circle is proportional to the total number of records at each point.

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Thresher shark Porbeagle Other

60 50

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40 30 20

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Hawaii

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Region

United Kingdom

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Mauritius

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10 Australia

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Fig. 15.2 Species of pelagic sharks for which there are year 2000 International Game Fish Association records (IGFA, 2000), by country or region. US North Atlantic includes the eastern United States except for Florida; the Caribbean includes Florida, the Bahamas, and Bermuda.

although Cape Moreton near Brisbane was once a popular shark-fishing destination and has held IGFA records for white sharks since the 1950s (IGFA, 2000; Schultz, 2000). Of the 72 IGFA records for pelagic sharks in Australia, 89% are from New South Wales, and the remainder are from South Australia, Victoria, and Tasmania (Fig. 15.1). The IGFA records from Australia are mainly mako and blue sharks (Fig. 15.2). Large sharks have been caught off southeastern Australia since rod-and-reel fishing for big fish became popular in the early 1900s (Pepperell, 1992). Pelagic sharks began to be caught in the 1960s as anglers started fishing farther offshore, and they now dominate the recreational shark catch (Stevens, 1984; Pepperell, 1992). Most shark fishing in Australia is done by members of 65 game fishing clubs associated with the Game Fishing Association of Australia (GFAA), particularly the 10 clubs along the New South Wales coast between Port Stephens and Bermagui (Pepperell, 1992; Murphy et al., 2002). Of the 7,879 recorded shark captures by these 10 clubs from 1961 to 1990, shortfin makos (28%) and blue sharks (19.5%) accounted for half the catch, and the rest were whalers (Carcharhinus spp., Carcharhinidae), hammerheads (Sphyrna spp., Sphyrnidae), grey nurse (Carcharias taurus, Carcharhinidae), white, and other sharks, including six threshers and one porbeagle (Pepperell, 1992). Blue sharks and shortfin makos dominated the catch in the area around Sydney, while whaler sharks dominated to the north and hammerheads to the south (Pepperell, 1992). A study of fishing tournaments from 1996 to 2000 in the same region found that sharks were targeted on 16% of the tournament boat-days, and that sharks were 11.7% of the tournament catch (in numbers). Makos compose 40.1% of the shark catch, and blue sharks 12.0% (Murphy et al., 2002). The average size of blues and shortfin makos landed increased between the 1960s and the 1980s, possibly because anglers were fishing farther offshore, but mainly because the GFAA’s voluntary minimum size limits have encouraged fishers to release the smaller

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sharks caught around Sydney in the spring (Pepperell, 1992). Between 1996 and 2000, for example, the average size of makos landed during tournaments was 136.2 kg, while the average size of tagged and released makos was 40.5 kg (Murphy et al., 2002). The GFAA minimum size was set at 45 kg in 1983 and increased to 60 kg in 1987, then to 80 kg in 1997 as the game fishing clubs became more interested in catch-and-release fishing (Pepperell, 1992, 1998; Murphy et al., 2002). Since the 1970s, a Gamefish Tagging Program has been run by New South Wales Fisheries in cooperation with the GFAA and the Australian National Sportfishing Association. Between 1993 and 1996, the program tagged 1,136 blue sharks, 2,596 shortfin makos, 56 threshers, and 8,489 other sharks, mainly hammerheads and whalers (GFAA, 2005). Of the sharks caught in tournaments from 1993 to 2000, 74.4% were tagged and released (Murphy et al., 2002). Current regulations from New South Wales Fisheries include a combined bag limit of five sharks and rays of all species per angler per day. This limit does not include white sharks, grey nurse sharks, and other prohibited species (New South Wales Fisheries, 2005).

New Zealand Game fishing in New Zealand began in 1915 (Francis, 1998), and there are currently around 60 game fishing clubs affiliated with the New Zealand Big Game Fishing Council (Cox and Francis, 1997; New Zealand Big Game Fishing Council, 2005). In the warm waters northeast of North Island, most big game fishing targets marlins and yellowfin tuna, and sharks tend to be released when caught because they are not a target species. However, blues and shortfin makos are caught in this region, as are the only thresher sharks caught in New Zealand (Cox and Francis, 1997; IGFA, 2000). Sharks are a primary target species for fishing clubs on the southeastern coast of North Island and around South Island (Cox and Francis, 1997). Blue sharks are the most common shark caught, although shortfin makos are the most likely to be retained. The IGFA records for New Zealand are mainly centered around the North Island (Fig. 15.1), and consist of mako and blue sharks, as well as some threshers and porbeagles (Fig. 15.2). According to a telephone, fishing diary, and boat-ramp survey of the New Zealand recreational fishery conducted in 1991–1994, recreational anglers take about 370,000 elasmobranchs annually (Francis, 1998). Most of these are coastal species: More than half are spiny dogfish (Squalus acanthias, Squalidae) and the rest are mainly school shark (Galeorhinus galeus, Triakidae) and rig (Mustelus lenticulatus, Triakidae). Because of the increase in catch-and-release fishing, the total landings of sharks have decreased. The only components of the recreational fishery to catch pelagic sharks are the fishing tournaments and the big game fishery, which is mainly associated with fishing clubs. Pelagic landings by game fish clubs peaked in 1981 at 1,248 sharks, of which about 60% were shortfin makos and 25% blue sharks. Landings between 1990 and 1996 were generally less than 600 pelagic sharks per year, mainly because fewer makos were landed (Francis, 1998). Sharks are also landed in shark tournaments, most of which have a minimum size limit of 40 kg for both blues and makos. The largest annual tournament, at Hawke Bay in northeastern South Island, attracts 600–700 anglers. About 99% of the sharks landed at tournaments are blue sharks and shortfin makos (C. Duffy, personal communication).

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Since 1975, the Ministry of Fisheries and the National Institute of Water and Atmospheric Research have been conducting a game fish tagging program in cooperation with recreational anglers (Hartill and Davies, 2000; Holdsworth and Saul, 2003). Between 1975 and 1990, 2,819 shortfin makos, 532 blue sharks, 12 threshers, and 1 oceanic whitetip (Carcharhinus longimanus, Carcharhinidae) were tagged by recreational anglers (Cox and Francis, 1997). The tagging program continues, and in the 2001–2002 season, 329 shortfin makos and 163 blues were tagged (Holdsworth and Saul, 2003). There are no restrictions on shark fishing in northern and central waters of New Zealand. However, in the South-East, Southland, and Sub-Antarctic Fishery Management Areas, the Ministry of Fisheries has imposed bag limits of one blue, one mako, one thresher, and one porbeagle per angler per day, as well as bag limits on some of the coastal shark species (New Zealand Ministry of Fisheries, 2005).

United States There are pelagic shark recreational fisheries on both the Atlantic and Pacific Coasts of the United States, and in Alaska and Hawaii (Fig. 15.1). The IGFA records on the Atlantic Coast are mainly blue sharks, while California holds more records than any other region for thresher sharks (Fig. 15.2). The Marine Recreational Fisheries Statistics Survey (MRFSS), managed by the National Marine Fisheries Service (NMFS), collects information on recreational fishing off the Pacific and Atlantic Coasts. This survey consists of dockside angler surveys to estimate the species composition of the recreational catch, combined with telephone surveys to determine the amount of total fishing effort, to yield total catch estimates (MRFSS, 2002). Recreational fishing for large sharks in the US Atlantic started to become popular in the 1960s, when the Cooperative Shark Tagging Program, now run by NMFS, began enlisting recreational fishermen to tag sharks (Kohler et al., 1998). Recreational shark fishing, both private and in tournaments, continued to grow in popularity throughout the 1970s and 1980s, partly in response to release of the movie Jaws in 1975 (Hueter, 1991; Schultz, 2000). Recreational shark landings peaked in the early 1990s, then declined as catch-and-release fishing became more popular and as the number of tournaments decreased (MRFSS, 2002; G. Skomal, personal communication; Skomal et al., 2008). According to the MRFSS, in 1999 fewer than 1% of the recreational fishing trips in the US Atlantic targeted elasmobranchs (MRFSS, 2002). The majority of these trips were made in the mid-Atlantic states (New York to Virginia, 97,000 trips) and the Gulf of Mexico (102,000 trips; MRFSS, 2002). Of the 5.7 million cartilaginous fish caught in 1999, about 2% were pelagic sharks, 32% coastal sharks (excluding spiny dogfish), 17% spiny dogfish, and 49% skates and rays. Most of the pelagic sharks were caught in waters off the mid- and North Atlantic states. Of the 89,000 blue sharks caught in 1999 in the US Atlantic and Gulf of Mexico, 31% were caught in North Atlantic states (Maine to Connecticut) and 67% were caught in mid-Atlantic states (New York to Virginia); 64% were caught in New York State alone. All of the 11,000 shortfin makos and the 6,000 thresher sharks caught in 1999 were caught in mid-Atlantic states. The 4,000 silky sharks (Carcharhinus falciformis, Carcharhinidae) caught in 1999 were all from South Atlantic and Gulf of Mexico states (MRFSS, 2002).

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The majority (91%) of the non-dogfish sharks caught in the US Atlantic and Gulf of Mexico were released alive (MRFSS, 2002). Thus, the recreational landings of pelagic sharks are low compared to those reported by the commercial fisheries. In 2001, total recreational mortality from the US Atlantic and Gulf of Mexico was only 950 blue sharks, 2,882 shortfin makos, and 4,070 silky sharks, according to NMFS statistics that include the MRFSS estimates, state of Texas estimates, and estimates from headboat (large party boat) surveys (Cortés and Neer, 2002; NMFS, 2003a). These data do not include delayed mortality of sharks that are released alive. However, physiological data and some radio tagging information indicate that survival rates may be quite high for live released pelagic sharks caught by recreational anglers (Skomal and Chase, 2002). Between 1962 and 1993, the NMFS Cooperative Shark Tagging Program tagged 329 bigeye threshers (Alopias superciliosus, Alopiidae), 48 common threshers, 3,457 shortfin makos, 73 longfin makos (Isurus paucus, Lamnidae), 457 porbeagles, 819 silky sharks, 542 oceanic whitetip sharks, 191 night sharks (Carcharhinus signatus, Carcharhinidae), and 60,856 blue sharks (Kohler et al., 1998; Kohler and Turner, 2008). Most sharks in the US Atlantic are managed by the NMFS under the Highly Migratory Species Fishery Management Plan (NMFS, 2000). The coastal states also regulate shark fishing within three miles of shore, but most state regulations are consistent with federal regulations (Camhi, 1998). Pelagic sharks have been subject to a bag limit since federal management began in 1993. The limit is currently one pelagic or coastal shark (excluding those coastal sharks with individual limits) per vessel per trip with a minimum size of 1.37 m. The catching of longfin makos, bigeye threshers, white sharks, and night sharks is prohibited (NMFS, 2003b). On the US Pacific Coast, most pelagic shark fishing takes place off southern California, which has had a large big game fishery since the first big tuna was taken off Catalina Island in 1898 (Reiger, 1999). In 1999, all of the 2,000 shortfin makos caught off the Pacific Coast were from southern California according to the MRFSS. Of the common threshers, 3,000 were caught off southern California and fewer than 1,000 off northern California. Sixteen thousand blue sharks were caught off southern California, 3,000 off northern California, and fewer than 1,000 each off Oregon and Washington. In southern California, 89% of the non-dogfish sharks caught were released alive (MRFSS, 2002). The California Department of Fish and Game has run a tagging program for sharks since 1983, in cooperation with both recreational anglers and commercial fishermen. Between 1983 and 1998, the program tagged 6,958 blue sharks, 2,674 shortfin makos, and 143 threshers (Camhi, 1999). The state of California imposes bag limits of two blue sharks, two threshers, and two shortfin makos per angler per day (Camhi, 1999). Pelagic sharks are included in the Pacific Fishery Management Council’s Fishery Management Plan for highly migratory species in US waters off California, Oregon, and Washington, but this federal plan does not impose any limits on the recreational fishery (Pacific Fishery Management Council, 2003). Alaska does not have a history of recreational fishing for pelagic sharks, but there is a developing recreational fishery for salmon sharks. In 2000, there were no IGFA records for salmon sharks; there is now one, in Alaska (IGFA, 2003). According to the charter boat logbooks collected by the state of Alaska, 581 salmon sharks were caught in southeastern Alaska in 1998, of which 82% were released, and 363 were caught in south-central Alaska,

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of which 72% were released (Camhi, 1999). The state of Alaska currently imposes a bag limit of one shark of any species per angler per day, and two sharks per angler per year (Camhi, 1999). In Hawaii and the US Pacific islands, pelagic sharks are not significant targets of the recreational big game fishery, which mainly targets marlins and tuna. Large threshers and makos are occasionally kept if they are caught by anglers targeting other game fish, but no agencies collect data on shark fisheries and there is no regulation of shark recreational fishing (Camhi, 1999).

United Kingdom The first big game shark fishery to develop in Europe was at Cornwall, which has held most of the IGFA records for porbeagle sharks since the 1950s (IGFA, 2000; Schultz, 2000) (Fig. 15.2). The Shark Angling Club of Great Britain (SACGB), a group of charter boat skippers based in East Looe, Cornwall, landed up to 6,000 blue, mako, porbeagle, and thresher sharks per year in the late 1950s (SACGB, 2003); the club now tags and releases all sharks. Catches have declined, but porbeagles are still caught around the Isle of Wight, off the coasts of Devon, Cornwall, and Wales, and off the west coast of Scotland (Fig. 15.1). Blue, mako, and thresher sharks are also caught seasonally throughout UK waters (Schultz, 2000). A national shark tagging program, run by shark anglers, was initiated in 2000, and 2,374 sharks were tagged between 2000 and 2002, including 97 blue sharks (of which five were recaptured) and 17 porbeagles (Drake et al., 2002). There is currently no management of shark recreational fishing in the United Kingdom, but most recreational fishing is catch-and-release (Drake et al., 2002).

Ireland The main pelagic target species in Ireland is the blue shark, and they are caught from Donegal around to Wexford in the summer months (Fitzmaurice and Green, 2000). The Central Fisheries Board of Ireland runs a sport fish tagging program that has been ongoing since 1970. Presently, all 70 Irish charter boats participate in the program, and 85% of sharks captured are released alive (P. Green, personal communication). The majority of pelagic sharks are caught from charter boats, so this represents most of the recreational fishery. From 1970 through 1999, the program tagged 30,500 fish, of which 15,747 were blue sharks and 56 were porbeagles (Fitzmaurice and Green, 2000).

Canada Atlantic Canada has managed pelagic sharks since 1995, with catch quotas in the commercial fishery and catch-and-release only for the recreational fishery (Department of Fisheries and Oceans, 2002). The recreational fishery began in 1994 and grew throughout the 1990s. Most sharks are caught in tournaments, and most are blues (with some makos and porbeagles, and a few threshers). All are released, except for those kept for research purposes at tournaments, which are mainly blue sharks (Department of Fisheries and Oceans, 2002). The numbers landed are small compared to the commercial fishery. For

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example, in 2000, 16 metric tons (t) of blue sharks were landed at tournaments (Canadian Shark Research Laboratory, 2005), compared to at least 1,108 t of landings and discards of blue shark in the Canadian commercial fisheries (Campana et al., 2002).

South Africa In South Africa, sharks are generally not desired by recreational fishermen, but they are caught in tournaments, where mainly coastal species are taken (Japp, 1999). South Africa holds four IGFA records (one mako and three thresher records; IGFA, 2000). However, most pelagic anglers discard sharks if they catch them (L. Compagno, personal communication). The recreational limit is 10 elasmobranchs per angler per day, excluding white sharks, which are protected (Penney et al., 1999). The Oceanographic Research Institute has been running a shark tagging program since 1983 and has tagged some pelagic sharks cooperatively with recreational fishermen (Pepperell, 1998).

Italy There are several IGFA records for thresher sharks from the Adriatic coast of Italy (IGFA, 2000), whose recreational fishery mainly targets blues and threshers. Some small blue sharks are released, but even the smallest thresher sharks tend to be retained (I. Bianchi, personal communication). A game fishing club called Big Game Italia tagged 453 blue sharks and 6 thresher sharks between 1987 and 1995 (N. Kohler, personal communication).

Other countries Although sharks are not specifically targeted in the Azores, some large mako, thresher, and blue sharks have been caught there (Schultz, 2000), including several records. Mauritius, the Bahamas, Bermuda, and Mexico also hold IGFA records (Figs. 15.1 and 15.2). Game fishing clubs or charter boat companies have reported catching pelagic sharks in Kenya, Thailand, Seychelles, Maldives, Malaysia, Indonesia, and the Philippines. Game fishing for pelagic sharks probably also occurs in other countries for which information is not readily available.

Conclusions Recreational fishing for big game sharks is growing in popularity in some areas, like Canada and New Zealand, and declining in others, like the United Kingdom. For all the recreational fisheries for which data are available, the trend is toward more catch-and-release fishing, often in cooperation with tagging and other research programs (Hueter, 1996; Pepperell, 1998). Because of this, recreational fishing does not generally cause high levels of mortality for most pelagic shark species, especially when compared to the catch and bycatch of commercial fisheries. Recreational fisheries are also a critical source of income for coastal communities that depend on tourism (e.g., Fisher and Ditton, 1993). Nevertheless, they have the potential to impose significant levels of mortality on pelagic shark populations that are

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already depleted. Therefore, greater monitoring of recreational fisheries would be desirable in many regions.

Acknowledgments Thanks to Irene Bianchi, Elinor Bullen, Merry Camhi, Steve Campana, Leonard Compagno, Nick Davies, Clinton Duffy, Sarah Fowler, Malcolm Francis, Peter Green, Lee Hulbert, Clive James, Nancy Kohler, Julian Pepperell, John Stevens, and Marino Vacchi for providing information about the shark fisheries in their regions. This work was funded by the Constantine S. Niarchos Fellowship in Marine Conservation, by The David and Lucile Packard Foundation, and by the Pew Charitable Trusts through a grant to the Pew Institute for Ocean Science. Thanks to Josh Drew, Merry Camhi, and two anonymous reviewers for comments on an earlier draft.

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Getty Thesaurus of Geographic Names (2005) www.getty.edu/research/conducting_research/vocabularies/tgn, accessed 6 February 2005. Grey, Z. (1976) Shark: The Killer of the Deep (ed. L. Grey). John Curley & Associates, South Yarmount, MA. Hartill, B. and Davies, N. M. (2000) New Zealand Billfish and Gamefish Tagging, 1998–99. NIWA Technical Report 79. National Institute of Water and Atmospheric Research, Wellington, New Zealand. Holdsworth, J. and Saul, P. (2003) New Zealand Billfish and Gamefish Tagging, 2001–02. New Zealand Fisheries Assessment Report 2003/15. National Institute of Water and Atmospheric Research, Wellington, New Zealand. Hueter, R. E. (1991) Survey of the Florida Recreational Shark Fishery Utilizing Shark Tournament and Selected Longline Data. Technical Report No. 232A. Mote Marine Laboratory, Sarasota, FL. Hueter, R. E. (1996) Catch/tag-and-release: The conservation option for recreational fishermen. Shark News. The Newsletter of the IUCN Shark Specialist Group 7, 7. International Game Fish Association (2000) World Record Game Fishes 2000. IGFA, Dania Beach, FL. International Game Fish Association (2003) World Record Game Fishes 2003. IGFA, Dania Beach, FL. International Underwater Spearfishing Association (2005) 20th Century Records List. www. freediver.net/iusa/records.php, accessed 6 February 2005. Japp, D. W. (1999) Management of elasmobranch fisheries in South Africa. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 199–217. Kohler, N. E. and Turner, P. A. (2008) Stock structure of the blue shark (Prionace glauca) in the North Atlantic Ocean based on tagging data. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Kohler, N. E., Kasey, J. G. and Turner, P. A. (1998) NMFS Cooperative Shark Tagging Program, 1962–93: An atlas of shark tag and recapture data. Marine Fisheries Review 60(2), 1–87. Marine Recreational Fisheries Statistics Survey (2002) National Marine Fisheries Service, Fisheries Statistics and Economics Division. www.st.nmfs.gov/st1/recreational/index.html, accessed 8 May 2002. Murphy, J. J., Lowry, M. B., Henry, G. W. and Chapman, D. (2002) The Gamefish Tournament Monitoring Program – 1993 to 2000. NSW Fisheries Final Report Series No. 38. Cronulla, New South Wales, Australia. National Marine Fisheries Service (2000) Final Fishery Management Plan for Atlantic Tunas, Swordfish, and Sharks, April 1999. NOAA/NMFS, Silver Spring, MD. National Marine Fisheries Service (2003a) 2003 Stock Assessment and Fishery Evaluation for Atlantic Highly Migratory Species. NOAA/NMFS, Silver Spring, MD. National Marine Fisheries Service (2003b) Final Amendment 1 to the Fishery Management Plan for Atlantic Tunas, Swordfish, and Sharks. NOAA/NMFS, Silver Spring, MD. New South Wales Fisheries (2005) New South Wales Recreational Saltwater Fishing Guide 2004–2005. www.fisheries.nsw.gov.au, accessed 6 February 2005. New Zealand Big Game Fishing Council (2005) www.fishing.net.nz/organisations/nzbgfc/index .cfm, accessed 6 February 2005. New Zealand Geographic Placenames Database (2005) www.linz.govt.nz/rcs/linz/pub/web/root/ core/Placenames/searchplacenames/index.jsp, accessed 6 February 2005. New Zealand Ministry of Fisheries (2005) www.fish.govt.nz, accessed 6 February 2005.

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Pacific Fishery Management Council (2003) Fishery Management Plan and Environmental Impact Statement for US West Coast Fisheries for Highly Migratory Species. www.pcouncil.org, accessed 6 February 2005. Penney, A. J., Mann-Lang, J. B., van der Elst, R. P. and Wilke, C. G. (1999) Long-term trends in catch and effort in the KwaZulu-Natal nearshore line fisheries. South African Journal of Marine Science 21, 51–76. Pepperell, J. G. (1992) Trends in the distribution, species composition and size of sharks caught by gamefish anglers off south-eastern Australia, 1961–90. Australian Journal of Marine and Freshwater Research 43(1), 213–225. Pepperell, J. G. (1998) Recreational fisheries for sharks. In: Shark Management and Conservation: Proceedings from the Sharks and Man Workshop of the Second World Fisheries Congress (eds. N. A. Gribble, G. McPherson and B. Lane). Brisbane, Australia, 2 August 1996. Department of Primary Industries, Brisbane, Australia. Reiger, G. (1999) Profiles in Saltwater Angling: A Tribute to Great Fish and Great Fishermen, 2nd edn. Silver Quill Press, Camden, Maine. Schultz, K. (2000) The World Atlas of Saltwater Angling. Lyons Press, New York. Shark Angling Club of Great Britain (2003) www.geocities.com/sacgb, accessed 12 December 2003. Skomal, G. and Chase, B. (2002) The physiological effects of angling on post-release survivorship in tunas, sharks, and marlin. In: Catch and Release in Marine Recreational Fisheries (eds. J. Lucy and E. Prince). American Fisheries Society, Bethesda, MD. Skomal, G., Babcock, E. A. and Pikitch, E. K. (2008) Case study: Blue and mako shark catch rates in US Atlantic recreational fisheries as potential indices of abundance. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Stevens, J. D. (1984) Biological observations on sharks caught by sport fishermen off New South Wales. Australian Journal of Marine and Freshwater Research 35, 573–590. US Geological Survey (2005) Geographic Names Information System. geonames.usgs.gov/pls/gnis/ web_query.gnis_web_query_form, accessed 6 February 2005.

Chapter 16

Case Study: Blue and Mako Shark Catch Rates in US Atlantic Recreational Fisheries as Potential Indices of Abundance Gregory Skomal, Elizabeth A. Babcock and Ellen K. Pikitch

Abstract Generalized linear models were used to derive indices of abundance for blue (Prionace glauca) and shortfin mako (Isurus oxyrinchus) sharks based on two components of the US Atlantic recreational fishery: (1) the private and charter boat recreational anglers covered by the Marine Recreational Fisheries Statistics Survey (MRFSS, 1981–2002) of the National Marine Fisheries Service and (2) Massachusetts shark tournaments (1991–2004). From the MRFSS data, blue shark catch per unit effort (CPUE) showed different trends for different regions, seasons, and fishing modes, implying that CPUE is not tracking blue shark abundance. Mako shark CPUE differed by mode for private versus charter boats, and showed no trend in either boat type. From the Massachusetts tournament data, blue shark CPUE showed different trends north and south of Cape Cod. Mako shark CPUE declined in the late 1990s in Massachusetts tournaments, then increased again in 2002. Key words: blue shark, mako shark, Prionace glauca, Isurus oxyrinchus, recreational fishing, shark tournaments, angling, game fishing, CPUE.

Introduction The blue shark (Prionace glauca, Carcharhinidae) and the shortfin mako (Isurus oxyrinchus, Lamnidae) are subject to extensive offshore recreational fisheries along the East Coast of the United States. From May through September each year, both species are sought by charter and private vessels, primarily from Virginia to Maine. Moreover, several big-game fishing tournaments that target these species are held annually in this region. The primary source of information about recreational fishing effort and catch in the United States is the Marine Recreational Fisheries Statistics Survey (MRFSS, 2002) of the National Marine Fisheries Service (NMFS). Total catch and effort data are also collected at shark tournaments by the Massachusetts Division of Marine Fisheries. We evaluate the Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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data from these two sources to determine whether it is possible to derive unbiased indices of abundance for blue and shortfin mako sharks.

Methods For both the MRFSS and Massachusetts tournament data, the raw catch per unit effort (CPUE) data were standardized using a general linear model (GLM) to account for the effects of different fishing areas and other factors that could affect catch rates. Once the effects of these explanatory variables were removed, the remaining year effect was assumed to be proportional to abundance (Babcock et al., 2000; Ortiz et al., 2000; Skomal et al., 2005). From the MRFSS intercept survey data, only trips that fished more than 4.8 km from shore were included in the analysis, as these trips were the most likely to catch blue and mako sharks. Blue shark catch rates (per angler-trip) were standardized using a delta lognormal GLM (Lo et al., 1992; Babcock et al., 2000; Ortiz et al., 2000; Skomal et al., 2005), in which the number of positive trips in each cell of the design is assumed to be binomial, and the catch per trip of trips with a positive catch is assumed to be lognormally distributed. The index of abundance of blue sharks is the product of the year effect for the binomial model and the year effect for the lognormal model. For mako sharks, only presence or absence in an angler-trip was standardized using a binomial GLM to derive an index of abundance because there were few trips reporting more than one shark caught. The MRFSS survey is stratified by year, fishing mode, sampling wave (2-month period), and state. For both species, we considered only strata for which there were substantial catches of blue and mako sharks. The explanatory variables considered were year (1981– 2002), sampling wave (May–June, July–August, September–October), fishing mode (private versus charter boats), and region (North Atlantic: Maine through Connecticut; mid-Atlantic: New York through Virginia; and for blue sharks only, South Atlantic: North Carolina through Florida), and all second- and third-order interactions between them. Models were chosen using the Akaike information criterion (AIC; Venables and Ripley, 1997), which weighs the number of parameters against the fit of the model to find the most parsimonious model. A more detailed description of the methods applied to the MRFSS data may be found in Babcock et al. (2000) and Skomal et al. (2005). For the tournament data for both blue and mako sharks, CPUE was measured as total catch divided by total boat-hours for each day of each tournament, owing to the lack of information on the number of anglers fishing in each boat (Browder and Prince, 1988). It was not necessary to use a delta lognormal model because there were few zero observations; CPUE was modeled with a log-link GLM appropriate for lognormal data (Venables and Ripley, 1997). The explanatory variables considered were year (1991–2004), region (Massachusetts: south of Cape Cod versus north of Cape Cod), and event (i.e., tournament) nested within region, so that the GLM was Ui,j,k,l
0.001  β0
βyr,i
βreg,j
βev,k
βyr,i,reg,j
εi,j,k,l where Ui,j,k,l is the CPUE in year i, region j, event k, and day l, with event being nested within region (Skomal et al., 2005). β0 is an intercept term, while βyr,i,, βreg,j, and βev,k are

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the parameters associated with the main effects of year i, region j, and event k. βyr,i,reg,j is the interaction effect between year i and region j; εi,j,k,l, is an error term. The test for significance of each effect was an F test appropriate for a log-link GLM (Venables and Ripley, 1997). Since the sample design is unbalanced, the order in which the explanatory variables are entered into the model affects their significance (Venables and Ripley, 1997). The explanatory variables were all categorical. We also entered year as a continuous variable to test whether there was a significant linear increase or decrease in the year effect over time, which might indicate a trend in biomass.

Results For blue shark catch rates from the MRFSS data, year, wave, mode, region, and many of the interactions between these variables were significant for both the presence/absence (Table 16.1(a)) and positive trip CPUE (Table 16.1(b)). Thus, the trend over the time series is different for each year, wave, mode, and region, and it is not likely that the model year effect tracks the abundance of blue sharks throughout the region. For mako shark presence/absence from the MRFSS data (Table 16.1(c)), year, wave, mode, and region were significant, as well as the year  mode, wave  region, and mode  region interactions. Since mode was the only variable with a significant interaction with year, the trend may be different in the two modes, but is the same in each region and wave (Fig. 16.1). For both fishing modes, the index was highly variable and showed no trend. In the GLM of blue shark catch rates from Massachusetts tournament data, year, region, and the year  region interaction were significant (Table 16.1(d)). There were not enough data points to include both the year  region interaction and tournament events in the model simultaneously. Event was not significant if region was already included in the model.

Table 16.1 Analysis of deviance for general linear models. (a) The best model (AIC) for blue shark presence/absence in the MRFSS data

Null Year Wave Mode Region Year  wave Year  mode Year  region Wave  mode Wave  region Mode  region Year  wave  mode Year  wave  region Wave  mode  region

Degrees of freedom

Deviance

21 2 1 2 42 21 42 2 4 2 42 84 4

542.11 7.86 175.09 2,382.15 175.84 149.61 83.26 39.96 100.21 3.27 261.24 227.93 17.10

Residual degrees of freedom

Residual deviance

395 374 372 371 369 327 306 264 262 258 256 214 130 126

4,298.21 3,756.09 3,748.23 3,573.14 1,190.99 1,015.16 865.55 782.29 742.33 642.12 638.85 377.62 149.69 132.59

Pr(Chi)

0.001 0.020 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.195 0.001 0.001 0.002 (Continued )

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Table 16.1 (Continued). (b) The best model (AIC) for blue shark CPUE in positive trips in the MRFSS data Degrees of freedom

Deviance

21 2 1 1 37 19 18 2 1 24 13

104.32 39.91 0.36 69.53 214.10 87.22 70.89 17.94 0.69 50.16 33.45

Null Year Wave Mode Region Year  wave Year  mode Year  region Wave  region Mode  region Year  wave  region Year  mode  region

Residual degrees of freedom

Residual deviance

1,248 1,227 1,225 1,224 1,223 1,186 1,167 1,149 1,147 1,146 1,122 1,109

1,772.05 1,667.73 1,627.82 1,627.46 1,557.92 1,343.83 1,256.61 1,185.72 1,167.78 1,167.09 1,116.93 1,083.48

F value

Pr(F)

3.89 15.62 0.28 54.43 4.53 3.59 3.08 7.02 0.54 1.64 2.01

0.001 0.001 0.596 0.001 0.001 0.001 0.001 0.001 0.464 0.028 0.017

(c) MRFSS mako sharks presence/absence Degrees of freedom Null Year Wave Mode Region Year  mode Wave  region Mode  region

21 2 1 2 21 4 2

Deviance

Residual degrees of freedom 395 374 372 371 369 348 344 342

82.07 21.86 51.03 569.78 48.74 24.85 23.68

Residual deviance 1,193.33 1,111.27 1,089.41 1,038.38 468.60 419.86 395.01 371.32

Pr(Chi)

0.001 0.001 0.001 0.001 0.001 0.001 0.001

(d) Tournament blue sharks Degrees of freedom Null Year Region Year  region

13 1 7

Deviance

14.82 5.33 7.60

Residual degrees of freedom

Residual deviance

68 55 54 47

37.73 22.91 17.58 9.98

F value

Pr(F)

5.60 26.15 5.33

0.001 0.001 0.001

(e) Tournament mako sharks

Null Year Region Region  year

Degrees of freedom

Deviance

13 1 7

1.12 0.39 0.06

Residual degrees of freedom

Residual deviance

68 55 54 47

2.37 1.26 0.87 0.81

F value

Pr(F)

4.96 22.37 0.53

0.000 0.000 0.808

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Standardized CPUE

0.05 0.04 0.03 0.02 0.01 0.00 1980

1985

1990 Year

1995

2000

1995

2000

(a)

Standardized CPUE

0.06 0.05 0.04 0.03 0.02 0.01 0.00 1980

1985

1990 Year (b)

Fig. 16.1 GLM standardized CPUE (2 SE) of mako sharks from MRFSS data, for the AIC best fit model, which includes interaction between year and fishing mode, for (a) charter boats and (b) private boats.

The significant interaction between region and year implies that there were different trends over time in the two regions (Fig. 16.2). There was no significant linear trend over time. In the GLM for mako shark CPUE from the tournament data, year and region were significant, but the year  region interaction was not significant (Table 16.1(e)). Tournament event was significant (p  0.019) even when year and region were already included in the model. The CPUE year effect declined in the late 1990s, but has increased since 2002 (Fig. 16.3). There was no significant linear trend over time.

Discussion Assessments of the status of pelagic sharks in the North Atlantic have been largely limited to the analysis of fishery-dependent CPUE data. Simpfendorfer et al. (2002) and Hueter and Simpfendorfer (2008) reported an 80% decline in standardized catch rates of male blue sharks from a fishery-independent longline survey in the western North Atlantic, but the catch data were restricted to the period of 1977–1994. For the recreational fishery, the MRFSS data are the most wide-ranging fishery-dependent data set and cover a relatively long time-series. However, the fact that the yearly trend in catch rates for blue sharks is

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Standardized CPUE

3.5 3 2.5 2 1.5 1 0.5 0 1990

2000

1995

2005

Standardized CPUE

Year (a) 4 3 2 1 0 1990

1995

2000

2005

Year (b) Fig. 16.2 GLM standardized CPUE (2 SE) of blue sharks from Massachusetts tournament data, for a model including year, region, and year  region as explanatory variables, for regions (a) south of Cape Cod and (b) north of Cape Cod.

Standardized CPUE

0.15

0.1

0.05

0 1990

1992

1994

1996

1998

2000

2002

2004

Year

Fig. 16.3 GLM standardized CPUE (2 SE) of mako sharks from Massachusetts tournament data, for a model including year and region as explanatory variables (south of Cape Cod).

influenced by fishing mode, time of year, and region implies that the year effect is probably not tracking blue shark abundance throughout the region. For mako sharks, each region and time of year has a similar trend, so that it is more likely that the year effect actually reflects changes in abundance over time. The index is quite variable, but does not appear to show a trend over time in either fishing mode. The fact that the MRFSS survey

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is not designed for rare-event species including pelagic sharks further complicates and argues against the utility of these data for assessing the status of blue and mako sharks. The Massachusetts tournament catch data for blue sharks showed different trends in the two regions. If both trends are tracking abundance, then they may be indicative of a regional shift in blue shark distribution. In their analysis of catch data from a western North Atlantic fishery-independent catch survey, Simpfendorfer et al. (2002) observed the highest blue shark CPUEs in a core area south of Cape Cod, which coincides with the southern region of the Massachusetts tournament effort. They reported a decline in male blue shark abundance in this region from 1977 to 1994. Subsequent to this period, Massachusetts tournament data demonstrated an increase in catch rates in this region for 1996–1998 followed by a decline for 1999–2002 (Fig. 16.2). There were no significant interactions with year in the mako tournament CPUE, implying that the yearly changes in mako CPUE reflect actual changes in mako shark abundance in this region. Together, the MRFSS and Massachusetts tournament data give some information about trends in abundance of blue and shortfin mako sharks in the western North Atlantic. The MRFSS data are quite variable, but the Massachusetts data seem to show trends in regional abundance over time, with blue sharks becoming increasingly common south of Cape Cod and less common north of Cape Cod in the 1990s, and shortfin mako sharks declining in the 1990s and increasing in abundance after 2001.

Acknowledgments This work was funded by the Constantine S. Niarchos fellowship in Marine Conservation, The David and Lucile Packard Foundation, the Pew Charitable Trusts through a grant to the Pew Institute for Ocean Science, and the Wildlife Conservation Society. The Massachusetts Sport Fishing Tournament Monitoring Program is funded, in part, by the Federal Aid in Sport Fish Restoration Act. This is Massachusetts Division of Marine Fisheries Contribution No. 12.

References Babcock, E. A., Pikitch, E. K. and McAllister, M. K. (2000) Catch rates of blue sharks (Prionace glauca) in the US Atlantic recreational fishery. ICCAT Collective Volume of Scientific Papers 51, 1850–1851. Browder, J. A. and Prince, E. D. (1988) Exploration of the use of tournament and dock catch and effort data to obtain indices of annual relative abundance for blue and white marlin 1972 through 1986. ICCAT Collective Volume of Scientific Papers 28, 287–299. Hueter, R. E. and Simpfendorfer, C. A. (2008) Case study: Trends in blue shark abundance in the western North Atlantic as determined by a fishery-independent survey. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Lo, N. C. H., Jacobson, L. D. and Squire, J. L. (1992) Indices of relative abundance from fish spotter data based on delta-lognormal models. Canadian Journal of Fisheries and Aquatic Sciences 49, 2515–2526.

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Marine Recreational Fisheries Statistics Survey (MRFSS) (2002) Atlantic and Gulf Intercept Data. National Marine Fisheries Service, Fisheries Statistics and Economics Division, Silver Spring, MD. Ortiz, M., Cramer, J., Bertolino, A. and Scott, G. (2000) Standardized catch rates by sex and age for swordfish (Xiphias gladius) from the US longline fleet 1981–1998. ICCAT Collective Volume of Scientific Papers 51, 1523–1551. Simpfendorfer, C. A., Hueter, R. E., Bergman, U. and Connett, S. M. H. (2002) Results of a fishery-independent survey for pelagic sharks in the western North Atlantic, 1977–1994. Fisheries Research 55, 175–192. Skomal, G., Babcock, E. A. and Pikitch, E. K. (2005) Indices of blue and mako shark abundance derived from US Atlantic recreational fishery data. ICCAT Collective Volume of Scientific Papers 58(3), 1034–1043. Venables, W. N. and Ripley, B. D. (1997) Modern Applied Statistics with S-Plus, 2nd edn. SpringerVerlag, New York.

Chapter 17

Catches of Pelagic Sharks by Subsurface Longline Fisheries in the South Atlantic Ocean during the Last Century: A Review of Available Data with Emphasis on Uruguay and Brazil Fabio H. V. Hazin, Matt K. Broadhurst, Alberto F. Amorim, Carlos A. Arfelli and Andres Domingo

Abstract Pelagic sharks are typically discarded as bycatch in subsurface longline fisheries in the South Atlantic Ocean. During the last 40 years of the 20th century, despite considerable fishing effort involving subsurface longline fleets from more than seven countries, there were few available data describing catch rates and relative abundances and distributions of the species caught. The majority of information came from small-scale longline fleets operating out of Brazil and Uruguay, where sharks historically have been landed and sold in local markets. This review shows that most of the large-scale temporal fluctuations in catch per unit of effort (numbers or weights of fish caught per 1,000 hooks per year) in these small-scale fisheries can be attributed to market-oriented factors (reflecting variabilities in consumer demand for various species) and the discovery of new fishing grounds. Toward the end of the century, gear-related changes also appear to have had an impact on catch rates. The lack of data precludes analyses of smaller-scale temporal and spatial trends in catches and relative abundances for nearly all species, except the blue shark (Prionace glauca). The available data indicate that such trends in the southwestern Atlantic Ocean can be largely attributed to movements associated with reproduction. We propose that the future effective management of pelagic sharks in the South Atlantic would be facilitated by implementation of more rigorous methods of obtaining information on catches and biological parameters for the key species, as well as an examination of the factors influencing gear selectivity. Key words: pelagic sharks, subsurface longlines, South Atlantic Ocean, bycatch, Brazil, Uruguay. Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Introduction The majority of fishing effort on pelagic sharks in the South Atlantic Ocean occurs in highseas, subsurface longline fisheries targeting tunas (Scombridae) and billfishes (Xiphiidae and Istiophoridae) (Bonfil, 1994). At least 11 species (Table 17.1) are caught incidentally (as bycatch) to the targeted species; in the majority of cases, these sharks are discarded at sea after their fins have been removed (ICCAT, 2001a). No attempts have been made to quantify the total catch of pelagic sharks in the South Atlantic, although Bonfil (1994) estimated that at least 2.3 million individuals or 76,000 metric tons (t) were caught and discarded in subsurface longline fisheries throughout the entire Atlantic Ocean in 1991. A definitive review of spatial and temporal variabilities in catches and relative abundances of pelagic sharks in the South Atlantic is difficult, owing to insufficient and/or unreliable data. The problems associated with obtaining data can be partially attributed to the highly migratory movements of the major species and their simultaneous exploitation by several international and coastal fishing fleets. A more serious limitation, however, is that although the majority of data are collated by official sources (i.e., the Food and Agriculture Organization of the United Nations, FAO, and the International Commission for the Conservation of Atlantic Tunas, ICCAT), they originate from logsheets completed by fishers, and these do not include accurate descriptions or quantifications of bycatch discarded at sea (Bonfil, 1994; Shotton, 1999). During the last century, several nations, including Japan, China, Korea, Spain, Taiwan, South Africa, Namibia, Brazil, and Uruguay, had fleets of subsurface longliners operating in the South Atlantic Ocean. With the exception of national vessels operating from Brazil and Uruguay, there are few data available on the catches of sharks by these fleets. Nevertheless, we offer brief reviews of all countries that fished in the South Atlantic during the 1900s, including any available information on catch compositions. Because some Table 17.1 Pelagic sharks caught in subsurface longline fisheries in the South Atlantic Ocean (ICCAT, 2001a). Family and scientific name

Common name

Alopiidae Alopias superciliosus Alopias vulpinus

Bigeye thresher Common thresher

Carcharhinidae Carcharhinus falciformis Carcharhinus longimanus Prionace glauca

Silky shark Oceanic whitetip Blue shark

Lamnidae Isurus oxyrinchus Isurus paucus Lamna nasus

Shortfin mako Longfin mako Porbeagle

Pseudocarchariidae Pseudocarcharias kamoharai

Crocodile shark

Squalidae Isistius brasiliensis Zameus squamulosus

Cookiecutter shark Velvet dogfish

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data are available for subsurface longline fisheries off Uruguay and Brazil, we provide more detailed discussion of chronological trends in these catches.

Catches of pelagic sharks by distant-water longline fleets Japan Japanese vessels were the first to begin subsurface longlining in the South Atlantic Ocean, during the mid-1950s. Initially, vessels targeted albacore (Thunnus alalunga, Scombridae) and yellowfin tuna (T. albacares), before shifting effort toward bigeye tuna (T. obesus) in the late 1970s. By 2000, this latter species made up more than half of the total catch of Japanese longliners operating in the Atlantic Ocean, with a total of 23,690 t caught in 1999 (ICCAT, 2001b). Japanese vessels have fished throughout the entire Atlantic Ocean since the late 1970s, although the majority of effort in the South Atlantic was concentrated in the Gulf of Guinea (from 0º to 20ºS and 10ºE to 20ºW). Annual fishing effort in the Atlantic Ocean ranged between 146 and 320 vessels, using between 40 and 90 million hooks (Nakano, 1993; ICCAT, 2001b). The bycatch of sharks by the Japanese fleet has been reported to include those species listed in Table 17.1, with the exception of the velvet dogfish (Zameus squamulosus, Squalidae) and cookiecutter shark (Isistius brasiliensis, Squalidae) (Nakano, 1993). According to Nakano (2000), the annual catch per unit of effort (CPUE) of pelagic sharks in the South Atlantic Ocean peaked at more than 8.0 sharks per 1,000 hooks in 1979, but remained relatively stable between 1981 and 2000, fluctuating between approximately 2.0 and 3.0 sharks per 1,000 hooks. These estimates should be treated with caution, however, since only 15–30% of vessels have provided data, and in some cases only included catches of high-valued species (Nakano, 1993). Nearly all species were discarded after their fins were removed.

China Chinese longliners primarily targeted bigeye tuna in the South Atlantic and landings rose from 63 t in 1992 to 7,347 t in 1999 (ICCAT, 2001c). Using data from onboard observers between 1994 and 1996, Xiao-jie and Zhan-qing (2000) reported that the shark bycatch includes large species such as the blue (Prionace glauca, Carcharhinidae) hammerhead (Sphyrna lewini, Sphyrnidae), shortfin and longfin mako (Isurus oxyrinchus and I. paucus, Lamnidae), oceanic whitetip (Carcharhinus longimanus, Carcharhinidae), and bigeye thresher (Alopias superciliosus, Alopiidae) sharks, and smaller species such as the crocodile shark (Pseudocarcharias kamoharai, Pseudocarchariidae). The combined annual CPUE of large species was estimated to be 3.18 sharks per 1,000 hooks; this group was mostly blue and mako sharks (87% and 10%, respectively). All blue sharks were finned and discarded, while the majority of makos were retained because of the higher prices for their meat.

Taiwan Taiwanese subsurface longliners began fishing for albacore in the Atlantic Ocean during the late 1960s (Hsu and Liu, 1993; Bonfil, 1994). This species remained a priority

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(17,377 t were caught in 1999; ICCAT, 2001c), although in the later 1990s, bigeye tuna was also targeted. Fishing effort remained fairly stable and involved 205 vessels in 1999 (ICCAT, 2001c). Shark catches historically were aggregated and annual yields between 1986 and 1991 were reported to be less than 1,500 t (Hsu and Liu, 1993). Observer-based programs initiated in 1998 (Chang and Chen, 1999) have indicated that the dominant species are the blue and thresher sharks (ICCAT, 2001c).

Korea Korean fishing effort in the Atlantic Ocean declined after 1977, and during the late 1990s was concentrated between 20ºN and 20ºS and directed toward bigeye tuna (124 t were caught in 1999; ICCAT, 2001c). The available data from ICCAT indicate that blue and mako sharks composed a large proportion of catches, although detailed information on composition is unavailable. Using effort and catch data from ICCAT (1992) and Hazin et al. (1990), Bonfil (1994) estimated that at least 190,245 sharks were caught in 1989, and 97% were discarded.

Spain Spanish subsurface longliners began fishing in the Atlantic Ocean, mostly to target swordfish (Xiphias gladius, Xiphiidae), during the early 1970s. Prior to 1988, vessels were restricted to the North Atlantic, before subsequent quota restrictions by ICCAT resulted in some shift of effort to the south. A total of 4,393 t of swordfish were caught in the South Atlantic in 1988, increasing to 11,290 t in 1995 (ICCAT, 2001c). Revised quota allocation in 1998 resulted in a decline in total catch to 4,079 t (ICCAT, 2001c). Some information on the catch compositions of pelagic sharks is available (e.g., Mejuto, 1985; Rey and Muñoz-Chápuli, 1991). As with other longline fisheries in the South Atlantic, the blue shark composed the majority of bycatch, and Mejuto (1985) estimated a discard rate close to 70% that was positively correlated with swordfish catches. Fishing strategy appeared to slightly change during the late 1990s, and depending on fluctuations in market prices and abundances, vessels alternately targeted swordfish and blue shark (Castro et al., 2000). In 1997 and 1998, bycatch landings from the entire Atlantic Ocean were 35,000 and 33,000 t (total weights), respectively (Castro et al., 2000). Of this catch, 99% consisted of pelagic sharks, and mostly blue and mako sharks, (85% and 10%, respectively, of total bycatch).

Catches of pelagic sharks by longline fleets from coastal nations Four coastal nations in the South Atlantic – Namibia, South Africa, Brazil, and Uruguay – had fleets of subsurface longliners during the last century. Vessels based out of Namibia and South Africa only started fishing in the 1990s, with 4 and 30 license holders, respectively (ICCAT, 1999; Penney and Griffiths, 1999; Kroese, 2000). Information on the bycatch of pelagic sharks from these fisheries is limited, although a preliminary assessment of catches from South African vessels revealed that the predominant species included blue and mako sharks (Penney and Griffiths, 1999). Blue sharks typically were discarded alive, while mako sharks were retained for sale. Brazil and Uruguay have established subsurface longline

Catches of Pelagic Sharks in the South Atlantic Ocean

217

fisheries and, in contrast to the majority of fleets described above, vessels have landed large proportions of their catches of pelagic sharks. Some historical catch data are available, facilitating assessments of trends in the catches and relative abundances of the main species, particularly the blue shark.

Uruguay Subsurface longlining began off Uruguay in 1969 with the acquisition of a Spanish vessel (Marín et al., 1998; Nion, 1999). This longliner targeted tunas for the following 5 years, after which there was no effort until 1981, when several Japanese vessels (37–55 m in length) were purchased and began fishing from Montevideo and La Paloma (Fig. 17.1). These vessels targeted bigeye tuna and swordfish using Japanese-style multifilament longlines (Suzuki et al., 1977) rigged with an average of 2,000 hooks. Several Chinese vessels also fished off Uruguay in 1984 and 1985, mainly targeting albacore. All vessels operating between 1981 and 1992 were equipped with onboard freezers. In 1992, the Japanese longliners were replaced with relatively smaller vessels (16–35 m in length) rigged with American- and Spanish-style longlines (see Domingo et al., 1996; Marín et al., 1998). These vessels began targeting swordfish and using monofilament mainlines with an average of 1,000 secondary lines (in clusters of five) rigged with lightsticks and baited with squid 70⬚ W

60⬚ W

50⬚ W

40⬚ W

Subarea I

30⬚ W

SP&SP Subarea II F de N

20⬚ W

0⬚ S

Natal Subarea III

10⬚ S

Brazil

20⬚ S Santos

30⬚ S Uruguay Montevideo La Paloma 40⬚ S

Fig. 17.1 Areas fished by the subsurface longline fleets operating from Brazil and Uruguay (F de N, Fernando de Noronha; SP & SP, Archipelago of St. Peter and St. Paul).

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Sharks of the Open Ocean

(Ilex argentinus). In contrast to the Japanese and Chinese vessels, catches were stored on ice and landed fresh.

Yearly trends in catches off Uruguay Since 1981, all vessels have been required to submit logsheets that include information on the numbers of hooks set and estimates of the dressed weights (headed, gutted, and finned) of fish caught during each fishing trip. In addition, some observer-based data were collected on 21 trips between 1993 and 1996 (Marín et al., 1998), and a national observer-based program was initiated in 1998. While all species listed in Table 17.1, with the exception of the cookiecutter shark and velvet dogfish, were recorded in catches, specific long-term data are available for only three species: blue, shortfin mako, and porbeagle (Lamna nasus, Lamnidae). The remaining sharks captured were mostly carcharhinid species and have been aggregated as a single group (termed “all other sharks combined”). One problem with using data collected from logsheets in this fishery is that some unknown proportion of bycatch was regularly discarded at sea (Domingo, 2000). It is difficult to determine, therefore, to what extent landed sharks reflect total catches or simply fluctuations in the commercial value of species. Also, some operators did not include effort data after 1992 and so subsequent values of the total number of hooks used per year are based on extrapolations (using total numbers of vessels and approximate hooks per vessel). Nevertheless, using the available effort (Table 17.2) and catch data from all vessels, we calculated yearly CPUE (weight of fish in kg per 1,000 hooks) to provide some information on changes in fishing strategy and relative abundances of key species and groups. Fluctuations in the annual CPUEs of total tunas, billfishes, and sharks (Fig. 17.2(a)) were closely aligned, indicating that for the most part distributions of these groups overlapped in the area fished (see also Marín et al., 1998). Owing to their relatively high commercial value, the porbeagle and shortfin mako made up the majority of sharks landed between 1981 and 1984 (Fig. 17.2(b)). A decline in the CPUE of total sharks between 1982 and 1986 can be attributed to low local market prices and possibly increased discarding at sea. The CPUE of porbeagle steadily declined after 1991, when Japanese vessels were replaced with smaller longliners. These latter vessels used ice (rather than freezers) and consequently had limited storage capabilities. It is likely that catches of porbeagle were discarded and not reported. Landed catches of shortfin mako shark generally remained low after 1984, possibly reflecting relatively low market prices. The blue shark was not recorded in catches until 1991, when the Japanese vessels were replaced by smaller longliners. Given that fishing areas remained the same, vessels operating prior to 1991 probably discarded their entire catches at sea (Domingo, 2000). Landed catches of blue sharks increased substantially after 1993. The slight reduction in the CPUE of blue sharks in 1995 corresponds to an increase in CPUE of “all other sharks combined,” and it is possible that a large proportion of blue shark catches were included in this category. In support of this, Marín et al. (1998) observed that from 43 and 49 longline sets sampled (between 1994 and 1996) in the Uruguayan exclusive economic zone and adjacent oceanic waters, respectively, the blue shark composed up to 60% of the total catch. Similarly, preliminary data collected between April 1998 and October 1999 as part of the national observer program showed that catches of blue shark

Catches of Pelagic Sharks in the South Atlantic Ocean

219

Table 17.2 Annual number of hooks used by all vessels operating off southern Brazil and Uruguay and by four vessels operating off northeastern Brazil. Year

Number of hooks Northeastern Brazil

1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998

– – – – – – – – – – – – 34,719 98,295 222,738 543,198 513,427 399,640 275,526 273,700 101,670 130,912 89,222 116,964 172,100 229,888 74,060 –

Southern Brazil 650,400 432,000 507,600 724,590 757,845 1,002,140 1,007,480 1,420,375 1,294,565 1,192,610 1,201,115 1,572,875 1,995,480 2,204,992 1,504,800 1,568,800 1,216,800 1,259,200 2,200,000 2,571,600 3,270,280 3,620,000 3,723,000 3,595,000 2,276,000 1,025,000 2,047,100 –

Uruguay – – – – – – – – – – 124,700 816,600 2,468,300 3,791,800 8,608,900 1,370,900 1,114,300 680,000 585,585 450,000 305,198 405,621 246,901 213,884 187,395 526,832 555,762 625,595

varied between 53% and 96% of the total shark catch and between 60% and 100% of the retained catch.

Brazil Two separate subsurface longline fisheries began off northeastern and southern Brazil in 1956 and 1958, respectively (Fig. 17.1), and involved Japanese-built vessels targeting tunas (Moraes, 1962, 1966). In the south, Japanese vessels fished adjacent oceanic areas until 1961. In 1965–1966, a Brazilian company began operating out of Santos with two national vessels (Arfelli and Amorim, 1988). By 1998, the number of vessels in this fleet had increased to 20 (16 national and 4 leased; Arfelli and Amorim, 2000). Off northeastern Brazil, the leased Japanese vessels ceased fishing in 1964. During 1976 and 1977, this fishery experienced a brief revival through the leasing of two Korean longliners, although there was no significant effort until 1983, when several local longliners began operating from Natal (Hazin et al., 1998). This fleet expanded throughout the following decade and by 2000 consisted of approximately 25 vessels. The configurations of longlines used

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2,500 Total tunas Total billfishes Total sharks

2,000

1,500

500

1991

1992

1993

1994

1995

1996

1997

1998

1991

1992

1993

1994

1995

1996

1997

1998

1990

1989

1988

1987

1986

1985

1984

1983

1982

0 1981

CPUE (weight of fish in kg/1,000 hooks)

1,000

(a) 1,531

Blue shark Shortfin mako shark Porbeagle shark All other sharks combined

400

300

200

100

1990

1989

1988

1987

1986

1985

1984

1983

1982

1981

0

Year (b) Fig. 17.2 Yearly CPUE estimates of (a) total tunas, billfishes, and sharks and (b) blue shark, shortfin mako, porbeagle, and all other sharks combined from the subsurface longline fleet operating off Uruguay from 1981 to 1998.

in these two fisheries have remained similar, with vessels setting at least 1,000 hooks, mainly baited with the Brazilian sardine (Sardinella brasiliensis), along mainlines up to 90 km in length. Japanese-style multifilament longlines (see Hazin et al., 1990, 1998, for details of gear used) were used until mid-1994 in the south (Arfelli, 1996) and 1996 in the

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northeast (Hazin et al., 1998), and then, as vessels began to target swordfish, these were replaced with configurations that included monofilament mainlines and secondary lines rigged with lightsticks (see Broadhurst and Hazin, 2001). Records describing catches of individual species of sharks began in 1971. As part of local management regulations, vessels operating off Brazil have been required to complete logsheets for each fishing trip. The information requested includes location of fishing grounds, numbers of hooks used, times of setting and retrieving the lines, and composition of catches. Some of these data were used in two quantitative studies that included analyses of large-scale spatial and temporal trends in the catches of pelagic sharks (Amorim et al., 1998; Hazin et al., 1998). Annual trends in CPUE are summarized below; in an attempt to isolate some of the factors influencing smaller-scale trends in catches, the results are then considered along with more specific work done on the distributions, relative abundances, and reproductive cycles of the key species.

Yearly trends in catches off southern Brazil Complete records of effort (Table 17.2) and catch (expressed in landed weights) data are available from all vessels that have operated in this fishery since 1971. All species listed in Table 17.1, with the exception of the velvet dogfish, have been captured (Amorim et al., 1998), although specific data are limited to blue, shortfin mako, and bigeye thresher sharks. The remaining pelagic sharks include carcharhinid species and have been aggregated as “all other sharks combined”; no data are available on fluctuations in the composition of this group. Data obtained from 21 observer-based trips indicate that the oceanic whitetip, night shark (C. signatus, Carcharhinidae), and shortfin mako frequently make up relatively large proportions of the catch (Amorim et al., 1998). Several factors influenced the annual landed catches of pelagic sharks off southern Brazil. Between 1971 and 1977, the main target species were yellowfin, bigeye, and albacore tunas (approximately 50% of the annual yield; Amorim et al., 1998) (Fig. 17.3(a)). Sharks were mostly avoided and discarded at sea (approximately 17% of landed catch; Amorim et al., 1998). An increase in the demand for shark meat and the establishment of local markets meant that after 1977 all species were landed. Depending on relative abundances of the main target species and market prices, between 1983 and 1994 pelagic sharks and particularly the blue shark were occasionally targeted, resulting in an increase in CPUEs (Fig. 17.3). By 1993, pelagic sharks composed 59% of the total landings (Amorim et al., 1998), with catches mostly dominated by the blue shark (Fig. 17.3(b)). Catches of all sharks then declined to about 15% of total catch after 1996 as all vessels began using monofilament longlines to target swordfish.

Yearly trends in catches off northeastern Brazil Comprehensive effort (Table 17.2) and catch data (in numbers of fish) are only available from four vessels that have operated in this fishery since 1983. Using these data, Hazin et al. (1998) provided a review of the fishery, including analyses of the relative abundance and distribution of pelagic sharks across general spatial and temporal scales. One difficulty with this work, however, was that prior to 1986 all sharks were collectively

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1,500

Total tunas Total billfishes Total sharks

1,200

Other fish combined

900

300

1987

1989

1991

1993

1995

1997

1987

1989

1991

1993

1995

1997

1985

1983

1981

1979

1977

1975

1973

0 1971

CPUE (weight of fish in kg/1,000 hooks)

600

Year (a) 600 Blue shark Mako shark All other sharks combined

500

400

300

200

100

1985

1983

1981

1979

1977

1975

1973

1971

0

Year (b) Fig. 17.3 Yearly CPUE estimates of (a) total tunas, billfishes, sharks, and other fish combined and (b) blue shark, mako, and all other sharks combined from the subsurface longline fleet operating off southern Brazil from 1971 to 1997.

grouped. Information on catches of individual species was recorded during the majority of subsequent trips, although it was not until 1990 that all vessels provided these data. A further limitation was that some species of Carcharhinidae, including the night, blacktip (Carcharhinus limbatus), silky (C. falciformis), and dusky (C. obscurus), were grouped

Catches of Pelagic Sharks in the South Atlantic Ocean

223

under the category of “gray sharks.” Catches of all other species were collectively analyzed as “all other sharks combined.” Yearly estimates of CPUE (number of sharks per 1,000 hooks) were calculated for species and groups and compared among three subareas, defined according to different oceanographic and biological conditions (Paiva and Le Gall, 1975; Hazin et al., 1998; Fig. 17.1). Pelagic sharks made up 54% of the total catch for the period examined, and included, in addition to most of the sharks listed in Table 17.1 (excluding the velvet dogfish and common thresher, cookiecutter, and porbeagle sharks), the night, blacktip, and dusky sharks (Hazin et al., 1990, 1994a, 1998, 2000a). Of these, the blue shark and those carcharhinid species grouped as gray sharks were the most dominant, representing 21% and 74%, respectively, of the total shark catch. The temporal trends in CPUEs of sharks shown in Fig. 17.4 can be attributed to variabilities in consumer demand for the various species and spatial movements of the fleet among areas of maximum abundances. For example, during the first 3 years of the fishery, tunas and billfishes were the main target groups (in oceanic areas), while sharks were avoided (Fig. 17.4(a)). An increase in the CPUE of total sharks between 1986 and 1987 was due to expansion in local markets for shark products (e.g., frozen fillets) and an increased awareness of their abundance and availability. From 1988 and during the first quarter of each year, vessels began targeting newly discovered schools of yellowfin tuna around the Archipelago of St. Peter and St. Paul (subarea II in Fig. 17.1). This resulted in some reduction in CPUE of gray sharks (1988–1990), due to a shift in effort away from their areas of maximum abundance (i.e., various shallow seamounts in subarea I). In 1992, an increase in the price of shark fins for international markets, combined with the discovery of large abundances of gray sharks around seamounts in subarea I, resulted in a substantial increase in CPUE of these species (Fig. 17.4(b)) and some drop in the CPUE of blue sharks. As with the subsurface longline fishery in the south, catches of gray sharks declined as vessels began using monofilament longlines (after 1996) to target swordfish. The inverse relationship between the CPUEs of gray and blue sharks after 1991 can be explained by species-specific differences among habitat preferences. For example, while the precise composition of gray sharks caught around seamounts in subarea I is unknown, the night shark has been recorded in relatively high abundances (Menni et al., 1995) and, from catches sampled during a reproductive study of this species, Hazin et al. (2000a) observed that more than 80% were juveniles and subadults. Since Travassos et al. (1999) showed that many seamounts in subarea I are characterized by considerable turbulence and possibly upwellings, which could facilitate primary production, it is conceivable that this area represents a nursery ground for the night shark. In contrast, because the blue shark is typically an oceanic species (Strasburg, 1958; Hazin et al., 1990), its relative abundance was low across such shallow areas and CPUE tended to be greater in the deeper, more oceanic regions of subareas II and III.

Factors influencing small-scale temporal and spatial trends in catches of blue shark The work described above was restricted to analyses of annual changes in fishing strategy, and little attempt was made to quantify any smaller-scale temporal and spatial trends in

224

Sharks of the Open Ocean

50

Total tunas Total billfishes Total sharks

40

Other fish combined

30

20

1997

1996

1995

1994

1993

1992

1991

1990

1989

1988

1987

1986

1985

1984

0 1983

CPUE (no. of fish/1,000 hooks)

10

(a) 50

Blue shark Gray shark All other sharks combined

40

30

20

10

1997

1996

1995

1994

1993

1992

1991

1990

1989

1988

1987

1986

0

Year (b) Fig. 17.4 Yearly CPUE estimates of (a) total tunas, billfishes, sharks, and other fish combined (1983–1997) and (b) blue shark, gray shark, and all other sharks combined (1986–1997) from the subsurface longline fleet operating off northeastern Brazil Shark.

catches. A lack of sufficient data precludes this sort of analysis for the majority of species, with the exception of the blue shark. Studies done on this species in the southwestern Atlantic Ocean suggest that such trends may be attributed to movements associated with reproduction (Hazin et al., 1990, 1994a, b; 2000a, b; Amorim, 1992). For example,

Catches of Pelagic Sharks in the South Atlantic Ocean

225

Amorim (1992) and Amorim et al. (1998) showed that blue sharks copulate off southern Brazil between November and February. Catches during this period usually comprise equal numbers of both sexes and are relatively low. In the south, females with fresh mating scars have been observed from November to March, but mainly from December to February, and during these later months catches are dominated by mature females. In the north, Hazin et al. (1990) observed that the highest relative abundance of blue sharks, mostly ovulating females, occurred in subarea II during the second quarter of the year. Using this information, Hazin et al. (2000b) hypothesized that females move northward from copulation areas off southern Brazil and Uruguay in late summer (i.e., February) to ovulate and fall pregnant off northeastern Brazil between April and June. Males probably remain segregated in the south, since large numbers are captured off southern Brazil and Uruguay during this period (Amorim et al., 1998). Relatively few females with large embryos are caught off northeastern Brazil after June, and it is likely that the majority move away, some possibly eastward into the Gulf of Guinea (Hazin et al., 2000b). In support of this, Castro and Mejuto (1995) recorded large numbers of females in early pregnancy in this area between June and August. In the absence of tagging studies, it is not possible to validate this hypothesized migration, although such movements do explain many of the small-scale temporal and spatial variabilities in relative abundances of this species in the southwestern Atlantic Ocean.

Management of pelagic sharks and directions for future research Information on species-specific life-history strategies and associated small-scale trends in spatial and temporal abundances, such as those discussed in the preceding sections, is needed to design and implement the future effective management of pelagic sharks in the South Atlantic Ocean. As a general example, if comprehensive data can be collected and used to elucidate patterns of movement, it might be possible to examine short-term spatial and temporal closures in an attempt to manage stocks. If some reduction in effort is required for the blue shark, this could involve limiting fishing to those specific places and times of large relative abundances (e.g., in subarea II during April and June). Similarly, if juveniles of species such as the night shark occur across well-defined spatial strata (e.g., at shallow seamounts) and a reduction in fishing mortality is required, it may be feasible to restrict longlining altogether in these areas. Unfortunately, for the majority of pelagic sharks caught throughout the South Atlantic Ocean, a lack of information precludes rational management involving closures in space and time. Detailed studies of the ecology of key species and more robust methods of quantifying bycatch need to be implemented. While it is apparent that logbooks and landed catches can provide some of the required information, the integrity of this type of fisherydependent data is difficult to assess (Kennelly, 1997), and in the majority of cases can be considered less than ideal. Previous studies have shown that the most reliable method for obtaining information about bycatch involves the long-term use of scientific observers recording data onboard commercial fishing vessels during normal operations (Saila, 1983; Kennelly, 1997). The need for observer-based programs has been recognized as a priority, and many countries recently have initiated such programs for their subsurface longline

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fleets operating in the South Atlantic (e.g., Marín et al., 1998; Chang and Chen, 1999; Kroese, 2000; ICCAT, 2001c). Coordination and standardization of sampling protocols are still required, however, to ensure compatibility of the data collected. While long-term quantification of spatial and temporal variabilities in bycatch and assessments of key biological parameters are required for the effective management of pelagic sharks, given current concern over rates of shark exploitation globally, it seems unwise not to examine the potential of more immediate bycatch reduction management strategies. One such option involves the design and development of modifications to current fishing gears and practices that improve selectivity for the target species. Little work has been published in the primary literature on factors influencing the selectivity of subsurface longlines in the South Atlantic (but see Broadhurst and Hazin, 2001). However, previous studies in other areas have shown that such factors can include: vertical distribution of hooks in relation to maximum abundance of target species (e.g., Rey and Muñoz-Chápuli, 1991; Boggs, 1992; Santana-Hernández et al., 1998; Bigelow et al., 1999); type and size of hooks (e.g., Huse and Fernö, 1990) and their spacing and numbers per cluster (e.g., Hamley and Skud, 1978; Hoey, 1995); setting methods (e.g., Løkkeborg, 1998); time and direction of set and soak duration (e.g., Løkkeborg and Pina, 1997); and, most importantly, the stimuli associated with bait (Løkkeborg and Johannessen, 1992; Løkkeborg and Bjordal, 1995; Broadhurst and Hazin, 2001). Given anecdotal evidence to suggest that subtle modifications to longline configurations (e.g., multifilament versus monofilament) may have an influence on the catch rates of sharks, manipulative experiments should be done to assess specific hypotheses about the factors that can influence the selectivity of subsurface longlines.

Conclusions During the last century, populations of pelagic sharks in the South Atlantic Ocean were subjected to various and mostly unknown intensities of fishing effort from subsurface longline fisheries. Limited data are available on rates of exploitation, mainly because, in the majority of fisheries, sharks were assigned a low priority relative to the economic value of targeted tunas and billfishes. In more recent years, an increased awareness of the potential ecological impacts associated with discarding unknown quantities of pelagic sharks has resulted in attempts at collecting the information required to facilitate appropriate management. As a first step, various countries have initiated observerbased programs aimed at providing data on spatial and temporal variabilities in bycatch. Relevant information on the life-history strategies of key species also needs to be collected. The data available from Brazil illustrate the potential benefits that such information may have for managing shark stocks. In the interim, it would be advantageous and precautionary to examine various modifications to longlines, including some assessments of likely factors influencing selectivity.

Acknowledgments Funding for this review was provided by the Comissão Interministerial para Recursos do Mar (CIRM) through the Programa Nacional de Avaliação do Potentcial Sustentável dos

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Recursos Vivos na Zona Econômica Exclusiva (REVIZEE) and the Conselho Nacional de Ensino e Pesquisa (CNPq). Thanks are extended to Norte Pesca for their assistance in compiling some of the catch data.

References Amorim, A. F. (1992) Estudo da biologia da pesca e reprodução do caçãoazul, Prionace glauca L. 1758, capturado no sudeste e sul do Brasil. Tese de Doutorado, Universidade Estadual Paulista, Rio Claro, São Paulo, Brasil, 205 pp. Amorim, A. F., Arfelli, C. A. and Fagundes, L. (1998) Pelagic elasmobranchs caught by longliners off southern Brazil during 1974–97: An overview. Marine and Freshwater Research 49, 621–632. Arfelli, C. A. (1996) Estudo da pesca e aspectos da dinâmica populacional de espadarte, Xiphias gladius L., 1758, no Atlântico Sul. Tese de Doutorado, UNESP, São Paulo, Brasil, 175 pp. Arfelli, C. A. and Amorim, A. F. (1988) Description of the Brazilian swordfish fishery in Santos. ICCAT Collective Volume of Scientific Papers 27, 315–317. Arfelli, C.A. and Amorim, A. F. (2000) Analysis of Santos (SP) longliners from southern Brazil (1997–99). ICCAT Collective Volume of Scientific Papers 50, 1359–1367. Bigelow, K. A., Boggs, C. H. and He, X. (1999) Environmental effects on swordfish and blue shark catch rates in the US North Pacific longline fishery. Fisheries Oceanography 8(3), 178–198. Boggs, C. H. (1992) Depth, capture time, and hooked longevity of longline-caught pelagic fish: Timing bites of fish with chips. Fishery Bulletin 90, 642–658. Bonfil, R. (1994) Overview of World Elasmobranch Fisheries. FAO Fisheries Technical Paper No. 341. FAO, Rome, Italy, 119 pp. Broadhurst, M. K. and Hazin, F. H. V. (2001) Influences of type and orientation of bait on catches of swordfish (Xiphias gladius) and other species in an artisanal subsurface longline fishery off northeastern Brazil. Fisheries Research 53, 169–179. Castro, J. A. and Mejuto, J. (1995) Reproductive parameters of blue shark, Prionace glauca, and other sharks in the Gulf of Guinea. Marine and Freshwater Research 46, 967–973. Castro, J., de la Serna, J. M., Macías, D. and Mejuto, J. (2000) Estimaciones científicas preliminares de los desembarcos de especies asociadas realizadas por la flota española de palangre de superficie en 1997 y 1998. ICCAT Collective Volume of Scientific Papers 51, 1882–1894. Chang, S. and Chen, C. (1999) Recent status of Atlantic longline fishery of Taiwan in 1997. ICCAT Collective Volume of Scientific Papers 49(4), 137–140. Domingo, A. (2000) Los elasmobraquios pelágicos capturados por la flota de longline Uruguaya. In: Consideraciones sobre la pesca incidental producida por la actividad de la flota atunera dirigida a grandes pelágicos (ed. M. Rey). Plan de Investigación Pesquera. INAPE-PNUD, Montevideo, Uruguay, pp. 14–23. Domingo, A., Mora, O. and Milessi, A. (1996) Capturas de tiburones pelágicos desembarcados por la flota atunera de Uruguay. ICCAT Collective Volume of Scientific Papers 46(4), 420–424. Hamley, J. M. and Skud, B. E. (1978) Factors affecting longline catch and effort. II. Hook spacing. International Pacific Halibut Commission Scientific Report 64, 15–50. Hazin, F. H. V., Couto, A. A., Kihara, K., Otsuka, K. and Ishino, M. (1990) Distribution and abundance of pelagic sharks in the south-western equatorial Atlantic. Journal of the Tokyo University of Fisheries 77(1), 51–64. Hazin, F. H. V., Boeckman, C. E., Leal, E. C., Lessa, R. P. T., Kihara, K. and Otsuka, K. (1994a) Distribution and relative abundance of the blue shark, Prionace glauca, in the southwestern equatorial Atlantic Ocean. Fishery Bulletin 92(2), 474–480.

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Hazin, F. H. V., Kihara, K., Otsuka, K., Boeckman, C. E. and Leal, E. C. (1994b) Reproduction of the blue shark Prionace glauca in the south-western equatorial Atlantic Ocean. Fisheries Science 60(5), 487–491. Hazin, F. H. V., Zagaglia, J. R., Broadhurst, M. K., Travassos, P. E. P. and Bezerra, T. R. Q. (1998) Review of a small-scale pelagic longline fishery off northeastern Brazil. Marine Fisheries Review 60(3), 1–8. Hazin, F. H. V., Lucena, F. M., Souza, T. S. A. L., Boeckman, C. E., Broadhurst, M. K. and Menni, R. C. (2000a) Maturation of the night shark, Carcharhinus signatus, in the south-western equatorial Atlantic Ocean. Bulletin of Marine Science 66(1), 173–185. Hazin, F. H. V., Pinheiro, P. P. and Broadhurst, M. K. (2000b) Further notes on reproduction of the blue shark, Prionace glauca, and a postulated migratory pattern in the South Atlantic Ocean. Ciência e Cultura, Journal of the Brazilian Association for the Advancement of Science 52, 114–120. Hoey, J. J. (1995) Bycatch in western Atlantic pelagic longline fisheries. In: Solving Bycatch: Considerations for Today and Tomorrow. Alaska Sea Grant College Program Report No. 96-03. University of Alaska, Fairbanks, AK, pp. 193–203. Hsu, C. C. and Liu, H. C. (1993) Status of Taiwanese longline fisheries in the Atlantic, 1991. ICCAT Collective Volume of Scientific Papers 40(2), 330–332. Huse, I. and Fernö, A. (1990) Fish behaviour studies as an aid to improved longline hook design. Fisheries Research 9, 287–297. ICCAT (1992) Data Record, Vol. 33. ICCAT, Madrid, Spain, 285 pp. ICCAT (1999) 1998 national report of Namibia. ICCAT Collective Volume of Scientific Papers 49(4), 423–426. ICCAT (2001a) 2000 Standing Committee on Research and Statistics Report of the Meeting of the Sub-committee on Bycatch. Document No. 20. ICCAT, Madrid, Spain, 9 pp. ICCAT (2001b) National Report of Japan. ICCAT Standing Committee on Research and Statistics Report No. 00/190. ICCAT, Madrid, Spain, 14 pp. ICCAT (2001c) Report of the Standing Committee on Research and Statistics, 12th Special Meeting of the Commission. ICCAT, Madrid, Spain. Kennelly, S. J. (1997) A framework for solving by-catch problems: Examples from New South Wales, Australia, the eastern Pacific and the Northwest Atlantic. In: Developing and Sustaining World Fisheries Resources: The State of Science and Management (eds. D. A. Hancock et al.). CSIRO Publishing, Collingwood, Victoria, Australia, pp. 544–550. Kroese, M. (2000) An overview of swordfish catches in the South African experimental pelagic longline fishery with emphasis on the south-western Atlantic Ocean. ICCAT Collective Volume of Scientific Papers 50, 1368–1374. Løkkeborg, S. (1998) Seabird by-catch and bait loss in long-lining using different setting methods. ICES Journal of Marine Science 55, 145–149. Løkkeborg, S. and Bjordal, Å. (1995) Size-selective effects of increasing bait size by using an inedible body on longline hooks. Fisheries Research 24, 273–279. Løkkeborg, S. and Johannessen, T. (1992) The importance of chemical stimuli in bait fishing– Fishing trials with presoaked bait. Fisheries Research 14, 21–29. Løkkeborg, S. and Pina, T. (1997) Effects of setting time, setting direction and soak time on longline catch rates. Fisheries Research 32, 213–222. Marín, Y. H., Brum, F., Barea, L. C. and Chocca, J. F. (1998) Incidental catch associated with swordfish longline fisheries in the south-west Atlantic Ocean. Marine and Freshwater Research 49, 633–639. Mejuto, J. (1985) Associated Catches of Sharks, Prionace glauca, Isurus oxyrinchus and Lamna nasus, with the NW and N Spanish Swordfish Fishery, in 1984. ICES C.M. 1985: H42. International Council for the Exploration of the Sea, Copenhagen, Denmark, 16 pp.

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Menni, R. C., Hazin, F. H. V. and Lessa, R. P. T. (1995) Occurrence of the night shark Carcharhinus signatus and the pelagic stingray Dasyatis violacea off northeastern Brazil. Neotrópica 41, 105–110. Moraes, M. N. (1962) Development of the tuna fishery of Brazil and preliminary analysis of the first three years’ data. Aquivos Estação de Biologia Marinha da Universidade do Ceará, Fortaleza 2(2), 35–37. Moraes, M. N. (1966) Que teria acontecido às pescarias de atuns? Revista Nacional da Pesca 51, 7–8. Nakano, H. (1993) A review of the Japanese fishery and research on sharks in the Atlantic Ocean. ICCAT Collective Volume of Scientific Papers 40(2), 409–412. Nakano, H. (2000) Updated standardized CPUE for pelagic sharks caught by Japanese longline fishery in the Atlantic Ocean. ICCAT Collective Volume of Scientific Papers 50, 1796–1804. Nion, H. (1999) La pesquería de tiburones en Uruguay con especial referencia al cazón (Galeorhinus galeus Linnaeus, 1758). In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 218–267. Paiva, M. P. and Le Gall, J. Y. (1975) Catches of tunas and tuna-like fishes in the longline fishery area off the coast of Brazil. Arquivos Ciências do Mar 15(1), 1–18. Penney, A. J. and Griffiths, M. H. (1999) A first description of the developing South African pelagic longline fishery. ICCAT Collective Volume of Scientific Papers 49(4), 162–173. Rey, J. C. and Muñoz-Chápuli, R. (1991) Relation between hook depth and fishing efficiency in surface longline gear. Fishery Bulletin 89, 729–732. Saila, S. B. (1983) Importance and Assessment of Discards in Commercial Fisheries. FAO Fisheries Circular No. 765. FAO, Rome, Italy, 62 pp. Santana-Hernández, H., Macías-Zamora, R. and Valdez-Flores, J. J. (1998) Selectivity of the longline system used by the Mexican fleet in the exclusive economic zone. Ciencias Marinas 24(2), 193–210. Shotton, R. (1999) Species identification practices of countries reporting landings of chondrichthyan fishes in the FAO “Nominal Catches and Landings” data base. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/2. FAO, Rome, Italy, pp. 904–920. Strasburg, D. W. (1958) Distribution, abundance and habitats of pelagic sharks in the central Pacific Ocean. Fishery Bulletin 58, 335–361. Suzuki, Z., Warashima, Y. and Kishida, M. (1977) The comparison of catches by regular and deep tuna longline gear in the western and central equatorial Pacific. Bulletin of the National Research Institute of Far Seas Fisheries 15, 51–89. Travassos, P. E. P. F., Hazin, F. H. V., Zagaglia, J. R., Rocha, R. A. and Schober. J. (1999) Thermocline structure around seamounts and islands of northeast Brazil. Archive of Fisheries and Marine Research 47(2/3), 211–222. Xiao-jie, D. and Zhan-qing, L. (2000) Deep longline bycatch in the tropical Atlantic Ocean. ICCAT Collective Volume of Scientific Papers 50, 1936–1940.

Chapter 18

Case Study: Blue Shark Catch-Rate Patterns from the Portuguese Swordfish Longline Fishery in the Azores Alexandre Aires-da-Silva, Rogério Lopes Ferreira and João Gil Pereira

Abstract Standardized blue shark (Prionace glauca) catch rates by the Mainland Portugal swordfish fleet operating in the Azores show an increasing trend from 1993 to 1998, suggesting improvement in fishing efficiency and/or a shift to blue sharks as the target species. Either hypothesis is supported by two asynchronous fishing seasons for swordfish and blue shark in the area, as well as the existing demand for shark meat in some European markets. This shift of fishing effort toward pelagic sharks occurs during times of low abundance of swordfish, particularly during the spring (i.e., the blue shark season). Length–frequency data collected during this season (March to May) suggest that the Azores represents an important nursery ground for North Atlantic blue sharks. The exploitation of this pelagic shark in the waters of the archipelago should therefore be regarded with caution, because young blue sharks are highly vulnerable in the spring months. Key words: Azores, blue shark, Prionace glauca, GLM, longline fishery, North Atlantic, nursery ground, Portuguese fishery, standardized CPUE, swordfish fishery.

Introduction The geographic position of the Azores archipelago in the middle of the North Atlantic Ocean, with immediate access to open oceanic waters, offers a unique potential for the exploitation of large pelagic fish populations, such as tuna, swordfish, and sharks. Pelagic shark catches in the Azores are predominantly associated with the Portuguese swordfish (Xiphias gladius, Xiphiidae) longline fishery. This fishery started in 1987 following the strong incentives for swordfish exploitation induced by the international meeting VII Azorean Fisheries Week, as well as by the good experimental fishing results obtained during 1985–1986 (Fernandes, 1987; Pousa, 1987). The Portuguese longline fleet targeting swordfish in the region has two main components: the Azores Region and Mainland Portugal fleets. A description of the physical Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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characteristics of each component can be found in Aires-da-Silva (2000). The former component lands mainly in Azorean ports and has already been described in detail (Simões and Marques-da-Silva, 1994). The Mainland Portuguese fleet comprises large-sized longliners with freezing capacity. These vessels operate around the archipelago year-round and land predominantly at the ports of Aveiro, Portugal, and Vigo, Spain. This chapter describes blue shark (Prionace glauca, Carcharhinidae) catch-rate patterns by this fleet, based on fishing logbooks kept by the longliners and observer data.

Fishing seasons The fishing logbooks of the Mainland Portugal longline fleet commonly report estimates of weight caught by set for the targeted swordfish and two shark species (blue shark and shortfin mako, Isurus oxyrinchus, Lamnidae). Analysis of logbook records (n ⫽ 6,947 longline sets) suggests that two fishing seasons can be identified for the longline fishery in the Azores: swordfish season and blue shark season. Catch per unit effort (CPUE) for blue shark and swordfish exhibit a pronounced seasonal nature and are out of phase with each other (Fig. 18.1). Higher catch rates of blue shark are obtained in the spring (March to June), while the high catch season for swordfish occurs in the fall (September to November). These tendencies are supported by observer data collected in a preliminary study (n ⫽ 77 sets) to investigate sea turtle bycatch of the longline fishery of the Azores (Ferreira, 1999; Prieto et al., 2000; Ferreira et al., 2001).

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Fig. 18.1 Monthly mean catch per unit effort (CPUE) of swordfish (SWO) and blue shark (BSH) in the Azores. Estimates are derived from fishing logbooks (1993–1998) and observer data (1998–1999). The vertical lines represent 95% confidence intervals.

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The logbook records show that the blue shark bycatch represents a major proportion of the total catches taken by the fishery, making up a minimum of 22% and a maximum of 86% during October and May, respectively. Shortfin mako catch levels are less than 5% of the total catches during the whole year. Discard levels are not reported in the logbooks and, for this reason, the catch-rate values presented here could be underestimated. It is possible that blue shark discards (dead or alive) occur, particularly when swordfish are abundant. This practice was rarely recorded during the preliminary observer study. However, a larger and continuing observer program is needed to better quantify discard levels.

Standardized catch rates Standardized yearly catch rates for blue sharks in Azorean waters were calculated for the period 1993–1998 from logbook reports by the Mainland fleet. A generalized linear model (GLM; McCullagh and Nelder, 1989; Maunder and Punt, 2004) was used to standardize the CPUE of sets with positive catches of blue sharks (n ⫽ 5,413). The GLM assumed a log-normal error distribution and the identity link was used. The model included, as main effects, the variables of year, month, season, and vessel. Three different fishing seasons were considered: a swordfish-targeted fishery (60–100% of swordfish in total catch), a multispecies fishery (40–60% of swordfish), and a fishery targeting blue sharks (⬍40% of swordfish). Table 18.1 presents results of the analysis of deviance, identifying the set of variables that best explained the variability. All the effects considered in the GLM were found to be significant (p ⬍ 0.001). Adding an interaction term between the year and season effects accounted for less than 1% of the variability; this interaction was not included in the GLM. The model explained 57% of the observed variability. Standardized CPUE for blue sharks shows a general increasing trend during the study period (Fig. 18.2). This increase suggests an improvement of the fishing efficiency and/or a shift to blue sharks as the target species. The existence of two out-of-phase fishing seasons for swordfish and blue shark in the Azores and demand for shark products in some European markets (Fleming and Papageorgiou, 1997) support either of these hypotheses. This shift of fishing effort toward pelagic sharks occurs during times of low swordfish abundance, particularly during the spring (i.e., the blue shark season). Table 18.1 Deviance analysis table of the GLM fitted to blue shark CPUE of positive sets.* Model structure Null Year Month Season Vessel Total deviance explained *

Degrees of freedom 5 11 2 22

Residual deviance 5,289.8 5,006.4 4,311.7 2,845.2 2,282.7

∆ deviance

% of total deviance

p value

283.4 694.7 1,466.5 562.5

9.4 23.1 48.8 18.7

⬍0.001 ⬍0.001 ⬍0.001 ⬍0.001

56.8

The residual deviance numbers show the decrease in deviance (∆ deviance) after each term was sequentially added to the model. The p values refer to the χ2 test (α ⫽ 5%) for the significance of each additional factor.

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Length–frequency samples Blue shark length–frequency data were collected during pelagic research cruises (Airesda-Silva, 1996; Marques-da-Silva et al., 1996) and in a preliminary fishing observer experiment carried out in the Azores (Ferreira, 1999; Prieto et al., 2000; Ferreira et al., 2001). Juvenile and subadult blue sharks (i.e., ⬍220 cm total length; Pratt, 1979) predominate in the waters of the archipelago during the spring (Fig. 18.3). This suggests that the Azores may be an important nursery ground for North Atlantic blue sharks during that time of the year.

Conclusions A new exploitation pattern has emerged in the swordfish longline fishery in the Azores, with seasonal shifting between a swordfish- and blue shark-targeted fishery and an increasing trend in blue shark yearly catch rates. The recent market demand for blue sharks in Europe represents a significant change from previous decades, when most blue shark catches were discarded owing to their low commercial value. Higher catches of blue sharks in the Azores are obtained during the spring, when the region appears to be an important nursery ground for the species. Given the reproductive limitations of shark populations as they relate to fisheries (Pratt and Casey, 1990), the emerging exploitation of blue sharks in the Azores clearly calls for increased monitoring and responsible management.

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0.12 March 1994 May 1998

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Acknowledgments We thank the crews of the R/V Arquipélago and an anonymous commercial longline vessel for logistical support provided during fieldwork. Two anonymous referees provided invaluable reviews. Furthermore, we express our thanks to Dr. Helen R. Martins for comments and suggestions.

References Aires-da-Silva, A. (1996) Contribution to the Knowledge of the Age and Growth of the Blue Shark, Prionace glauca (Carcharhinidae), in the North Atlantic. Undergraduate thesis, Universidade do Algarve, Faro, Portugal (in Portuguese; abstract, tables, and figures in English). Aires-da-Silva, A. (2000) The swordfish fishery in the Azores: An overview. In: Workshop to Design an Experiment to Determine the Effects of Longline Gear Modification on Sea Turtle Bycatch Rates (eds. A. B. Bolten, H. R. Martins and K. A. Bjorndal). NOAA Technical Memorandum NMFS-OPR-19. NOAA/NMFS, Silver Spring, MD, pp. 3–16. Fernandes, L. (1987) Pesca experimental de espadarte nos Açores com palangre de deriva. VII Semana das Pescas dos Açores 1987, 121–126 (in Portuguese). Ferreira, R. L. (1999) Caracterizção das capturas acessórias da pesca dirigida ao espadarte (Xiphias gladius) nos Açores. Undergraduate thesis, Universidade do Algarve, Faro, Portugal (in Portuguese; abstract in English).

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Ferreira, R. L., Martins, H. R., Aires-da-Silva, A. and Bolten, A. B. (2001) Impact of swordfish fisheries on sea turtles in the Azores. Arquipélago Life and Marine Sciences 18A, 75–79. Fleming, E. H. and Papageorgiou, P. A. (1997) Shark Fisheries and Trade in Europe. TRAFFIC Europe, Brussels, Belgium, 78 pp. Marques-da-Silva, H. M., Aires-da-Silva, A. and Simões, P. (1996) Relatório do cruzeiro de grandes pelágicos realizado durante o Outono 93/Primavera 94 nos Açores (ARQPAÇO-01-O93/P94). Arquivos do DOP, Série Cruzeiros 1 (in Portuguese; abstract in English). Maunder, M. N. and Punt, A. E. (2004) Standardizing catch and effort data: A review of recent approaches. Fisheries Research 70, 141–159. McCullagh, P. and Nelder, J. A. (1989) Generalized Linear Models, 2nd edn. Chapman and Hall, London, UK. Pousa, A. G. (1987) Como se trabaja al espadarte. VI Semana das Pescas dos Açores 1986, 269–271 (in Spanish). Pratt Jr., H. L. (1979) Reproduction in the blue shark, Prionace glauca. Fishery Bulletin 77(2), 445–470. Pratt Jr., H. L. and Casey, J. G. (1990) Shark reproductive strategies as a limiting factor in directed fisheries, with a review of Holden’s method of estimating growth parameters. In: Elasmobranchs As Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries (eds. H. L. Pratt Jr., S. H. Gruber and T. Taniuchi). NOAA Technical Report NMFS 90. NOAA/NMFS, Silver Spring, MD, pp. 97–109. Prieto, R., Ferreira, R. and Aires-da-Silva, A. (2000) Turtle bycatch study in the longline fisheries of the Azores. In: Workshop to Design an Experiment to Determine the Effects of Longline Gear Modification on Sea Turtle Bycatch Rates (eds. A. B. Bolten, H. R. Martins and K. A. Bjorndal). NOAA Technical Memorandum NMFS-OPR-19. NOAA/NMFS, Silver Spring, MD, pp. 22–28. Simões, P. and Marques-da-Silva, H. (1994) Caracterização da pesca de espadarte (Xiphias gladius) em águas Açoreanas: Período 1987–92. XIII Semana das Pescas dos Açores 1994, 203–222 (in Portuguese).

Chapter 19

Case Study: Trends in Blue Shark Abundance in the Western North Atlantic As Determined by a Fishery-Independent Survey Robert E. Hueter and Colin A. Simpfendorfer

Abstract The blue shark (Prionace glauca) is the most abundant large, pelagic shark inhabiting upper oceanic waters. Because of its widespread distribution and relatively high fecundity, the blue shark has been depicted by some as being more resistant to the impacts of fishing pressure than other shark species. To test this hypothesis, we investigated historical trends in the abundance of blue sharks in the western North Atlantic during a period in which commercial and recreational catches of pelagic sharks were substantial. We used catch and effort data from the R.V. Geronimo, a fishery-independent longliner that operated consistently in the summer months from 1977 to 1994 in US continental shelf waters south of Massachusetts, Rhode Island, and New York. The catches included juveniles and adults of both sexes, but very few adult females. When catch per unit of effort was analyzed using a generalized linear model, male blue sharks showed an approximately 80% decline between the mid-1980s and the early 1990s. A significant change in female catch rates could not be demonstrated, primarily because of the lower numbers of females in the catch. These results suggest that a dramatic decline occurred in the abundance of male blue sharks inhabiting a portion of the western North Atlantic. The broader significance of this finding is not known, but it challenges the common view that the relatively prolific nature of these sharks makes them immune to the effects of overfishing. Key words: blue shark, Prionace glauca, pelagic shark abundance, CPUE, fisheryindependent survey, CPUE, western North Atlantic.

Introduction Blue sharks (Prionace glauca, Carcharhinidae) are a broadly distributed, abundant species of large pelagic shark. They are found in all temperate and tropical oceanic waters, making Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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them perhaps the widest-ranging chondrichthyan fish (Compagno, 1984). They also may be the most prolific species of requiem shark, with average litter sizes of about 25–50 pups depending on geographic region (Strasburg, 1958; Pratt, 1979; Nakano, 1994; Castro and Mejuto, 1995); as many as 135 pups have been reported in a single litter (Gubanov, 1978). Because of their wide distribution, relatively high fecundity, and reported faster growth rate compared to other, slower-growing carcharhinids (Stevens, 1975; Skomal, 2003), blue sharks have been characterized by some fishery interests as being relatively invulnerable to the effects of overfishing (e.g., Spalding, 1999). These interests have promoted the blue shark as an exception to the rule that sharks in general are inherently susceptible to the impacts of intensive fishing. We wanted to test this hypothesis by examining a relatively long time-series of blue shark abundance in the western North Atlantic. One of the challenges to determining abundance of a pelagic species such as the blue shark is obtaining standardized catch data for a fixed region, using consistent methods over a significant period of time. Fisheryindependent data are usually preferred over fishery-dependent data, because they do not have many of the biases associated with data from commercial or recreational fishers (e.g., changing gear, methods, and targeting practices over time).

Survey catch records Beginning in 1974, a small-scale, fishery-independent longlining operation was conducted on a regular basis by the research vessel R.V. Geronimo in coastal and offshore waters of the North Atlantic. The boat’s primary research activity from the mid-1970s through the late 1990s was tagging blue sharks for the Cooperative Shark Tagging Program of the National Marine Fisheries Service. The longline gear deployed on Geronimo was a standard floating “Yankee” rig of 80–140 baited gangions, with a mean set time of 4 hours. The boat’s fishing operations and data collection procedures remained basically unchanged from 1977 to 1994 (Simpfendorfer et al., 2002). We analyzed the Geronimo catch records to look for trends in catch per unit of effort (CPUE) of blue sharks in the western North Atlantic from the mid-1970s to the mid1990s. We used data from longline sets in the months of June, July, and August that were conducted in continental shelf waters from Maine to Virginia along the US eastern seaboard, because that was the most consistent portion of Geronimo’s operations. The majority of the sets were made in shelf waters south of Massachusetts, Rhode Island, and New York (Fig. 19.1). A total of 132,496 hook-hours were included in the data set, resulting in a total catch of 4,860 blue sharks from 1977 to 1994. These included 3,334 males and 1,526 females, for a sex ratio of 1:0.5. Approximately 80% of the males were immature, but over half were within 40 cm, and over one-third within 20 cm, of size at sexual maturity (183 cm; Pratt, 1979). More than 99% of the females were immature (185 cm; Pratt, 1979), but almost half fell within the “subadult” size range (145–185 cm) of nearly sexually mature females as designated by Pratt (1979). Therefore, this area of the western North Atlantic during the summer appears to be dominated by older juvenile male and female blue sharks. Cortés (1999) concluded that increased mortality of older juveniles, as opposed

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76º

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Fig. 19.1 Locations of sets made by the R.V. Geronimo in the study area during June, July, and August 1977–1994. The small box is expanded in the lower right. (Reprinted from Simpfendorfer et al., 2002, with permission of Fisheries Research.)

to young juveniles or adults, has the greatest impact on populations of another requiem shark, the sandbar shark (Carcharhinus plumbeus, Carcharhinidae). Since there is no evidence that this would be different for the blue shark, relative abundance of the predominantly older juvenile sharks in the Geronimo survey may be an important indicator of the status of the blue shark stock in the western North Atlantic.

Trends in abundance To examine trends in relative abundance of these sharks, we divided the number of blue sharks caught in each set by the fishing effort to yield the CPUE (in sharks per 1,000 hookhours), which was then log transformed (ln(CPUE
1)) to normalize the data. CPUE data were calculated separately for male and female sharks, since previous studies have shown major differences in the occurrence and movements of the sexes in the western North Atlantic (e.g., Pratt, 1979; Kohler et al., 1998). Standardized catch rates were calculated using a generalized linear model (GLM) with years, months, and time of day as factors (Simpfendorfer et al., 2002). CPUE values for individual sets ranged from 0.0 to 253.6 sharks per 1,000 hook-hours for male blue sharks and from 0.0 to 190.5 sharks per 1,000 hook-hours for females. In the early years (1977–1978), annual catch rates were low, but they increased and remained relatively steady between 1979 and 1985 (the catch rate was high in 1987, but the sample size

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was small). Catch rates then fell and remained low through 1994. The magnitude of the decline in male catch rates over time can be seen in the decrease in annual mean values, which showed an approximately 80% decline from the mid-1980s to the early 1990s (Fig. 19.2). Annual catch rates of female blue sharks suggested a decrease in the mid-1980s, but the sparse data did not allow a definitive conclusion on female abundance. This significant downward trend in male catch rates is similar to that for males and females combined reported by Cramer (2000) and Baum et al. (2003) for bycatch data from the US North Atlantic pelagic longline fleet, which experienced decreasing catches of blue sharks during the late 1980s and then low but stable catches in the 1990s. However, south of the Geronimo survey area off the southeastern United States, the US pelagic longline fleet caught predominantly female blue sharks in the mid-1990s (Beerkircher et al., 2008), and thus the relationships between the Geronimo data and the US fleet data are unclear. In contrast, the lack of a clear trend in Geronimo’s female catch rates more closely resembles results reported by Nakano (2000) from logbooks of Japanese longliners operating in the North Atlantic. Since Nakano’s data came mostly from the central North Atlantic, where females were more prevalent, his results possibly reflect mostly female catch rates. These differences in trends between the US and Japanese catches of blue sharks in the North Atlantic remain unexplained. From these various results, and from catch data by size in the Geronimo data set (Simpfendorfer et al., 2002), we conclude that a combination of effects occurred in the male blue shark population of the western North Atlantic off the northeastern

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US coast: The less abundant mature male sharks became even scarcer after the mid-1980s, and at the same time the more numerous large, juvenile males were depleted in the region. Reasons for these declines are not clear, and commercial and recreational effort and catch data for blue sharks are difficult to find for the specific period and location of the Geronimo survey, but the signs point toward a combination of bycatch and directed overfishing. Anderson (1985) documented substantial catches of pelagic sharks (up to 10,000 metric tons (t)/year), including blue sharks, in US swordfish longline, Japanese tuna longline, and other pelagic commercial fisheries in the western North Atlantic from 1960 to 1981. At the same time, the estimated pelagic shark catch by US recreational fishermen from Maine to Virginia (a zone that overlaps the study area of the Geronimo survey) steadily increased from 992 t in 1965 to 5,367 t in 1980 (Anderson, 1985). It is possible that the increasing bycatch of pelagic sharks in the US swordfish fishery, the stable but continuous bycatch of pelagic sharks in the Japanese tuna fishery, and the increasing catch of pelagic sharks in the US recreational fishery all combined to take an aggregate toll on the population of blue sharks in the western North Atlantic. A lag time of a decade (post-1977 to post-1987) for these effects to manifest themselves is not unreasonable considering the life-history characteristics of blue sharks and the fact that the Geronimo survey caught predominantly immature sharks, which may have been impacted by recruitment overfishing in a specific part of their range. The results of this analysis need to be interpreted in the broader context of the North Atlantic blue shark population, which is widely distributed and sexually segregated, and has complex migratory patterns. Whether these results represent an indicator of a localized stock depletion – perhaps the first documented case for a pelagic species (Hueter et al., 2005) – or signs of a broader decline in abundance are unclear from these data. Regardless of whether the depletion was localized or not, our findings challenge the supposition that these pelagic sharks are impervious to the impacts of overfishing. Blue shark fecundity is high relative only to that of other sharks; other marine resources, such as bony fishes and invertebrates, have fecundities that are orders of magnitude higher than that of the blue shark. Our conclusions support the listing of the blue shark as an exploited species with a limited reproductive potential and other life-history characteristics that make it especially vulnerable to overfishing, as proposed by Camhi et al. (1998), Castro et al. (1999), and others. The Geronimo survey data demonstrate that population declines in blue sharks can and do occur, and strongly support a precautionary course in managing exploitation of blue shark populations in the open ocean.

Acknowledgments We are indebted to Capt. Stephen Connett, the crew and students of R.V. Geronimo, St. George’s School of Newport, Rhode Island, and Jack Casey, Wes Pratt, and Nancy Kohler of the NOAA/NMFS Narragansett Laboratory. Ulrika Bergman extracted the logbook data, and Jon Perry of Mote Marine Laboratory and Grayson Wood of the NOAA CoastWatch Program, Northeast Region, assisted with mapping. We thank Fisheries Research for permission to reprint Fig. 19.1. This study was funded in part by a NOAA/NMFS grant to R.E.H. and by Mote Marine Laboratory.

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References Anderson, E. D. (1985) Analysis of Various Sources of Pelagic Shark Catches in the Northwest and Western Central Atlantic Ocean and Gulf of Mexico with Comments on Catches of Other Large Pelagics. NOAA Technical Report NMFS 31. NOAA/NMFS, Silver Spring, MD, 14 pp. Baum, J. K., Myers, R. A., Kehler, D. G., Worm, B., Harley, S. J. and Doherty, P. A. (2003) Collapse and conservation of shark populations in the northwest Atlantic. Science 299, 389–392. Beerkircher, L. R., Cortés, E. and Shivji, M. S. (2008) Case study: Elasmobranch bycatch in the pelagic longline fishery off the southeastern United States, 1992–1997. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Camhi, M., Fowler, S., Musick, J., Bräutigam, A. and Fordham, S. (1998) Sharks and Their Relatives: Ecology and Conservation. IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, 39 pp. Castro, J. A. and Mejuto, J. (1995) Reproductive parameters of blue shark, Prionace glauca, and other sharks in the Gulf of Guinea. Marine and Freshwater Research 46, 967–973. Castro, J. I., Woodley, C. M. and Brudek, R. L. (1999) A Preliminary Evaluation of the Status of Shark Species. FAO Fisheries Technical Paper No. 380. FAO, Rome, Italy, 72 pp. Compagno, L. J. V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 2. Carcharhiniformes. FAO Fisheries Synopsis No. 125. FAO, Rome, Italy, pp. 251–655. Cortés, E. (1999) A stochastic stage-based population model of the sandbar shark in the western North Atlantic. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 115–136. Cramer, J. (2000) Large pelagic logbook catch rates for sharks. ICCAT Collective Volume of Scientific Papers 51(6), 1842–1848. Gubanov, Y. P. (1978) The reproduction of some species of pelagic sharks from the equatorial zone of the Indian Ocean. Journal of Ichthyology 18, 781–792. Hueter, R. E., Heupel, M. R., Heist, E. J. and Keeney, D. B. (2005) Evidence of philopatry in sharks and implications for the management of shark fisheries. Journal of Northwest Atlantic Fishery Science 35, 239–247. Kohler, N. E., Casey, J. G. and Turner, P. A. (1998) NMFS Cooperative Shark Tagging Program, 1962–93: An atlas of shark tag and recapture data. Marine Fisheries Review 60, 1–87. Nakano, H. (1994) Age, reproduction and migration of blue shark in the North Pacific Ocean. Bulletin of the National Research Institute of Far Seas Fisheries 31, 141–219. Nakano, H. (2000) Updated standardized CPUE for pelagic sharks caught by Japanese longline fishery in the Atlantic Ocean. ICCAT Collective Volume of Scientific Papers 51(6), 1796–1803. Pratt, H. L. (1979) Reproduction in the blue shark, Prionace glauca. Fishery Bulletin 77, 445–470. Simpfendorfer, C. A., Hueter, R. E., Bergman, U. and Connett, S. M. H. (2002) Results of a fishery-independent survey for pelagic sharks in the western North Atlantic, 1977–1994. Fisheries Research 55, 175–192. Skomal, G. B. (2003) Age and growth of the blue shark (Prionace glauca) in the North Atlantic Ocean. Fishery Bulletin 101, 627–639. Spalding, S. (1999) Blue shark: A common offshore species. Hawaii Fishing News, Western Pacific Regional Fishery Management Council, August 1999, pp. 24–25. Stevens, J. D. (1975) Vertebral rings as a means of age determination in the blue shark (Prionace glauca L.). Journal of the Marine Biological Association of the United Kingdom 55, 657–665. Strasburg, D. W. (1958) Distribution, abundance, and habits of pelagic sharks in the central Pacific Ocean. Fishery Bulletin 58, 335–361.

Chapter 20

Case Study: Elasmobranch Bycatch in the Pelagic Longline Fishery off the Southeastern United States, 1992–1997 Lawrence R. Beerkircher, Enric Cortés and Mahmood S. Shivji

Abstract Observer data from the US pelagic longline fishery were examined to describe the characteristics of elasmobranch bycatch off the southeastern coast of the United States from 1992 to 1997. Elasmobranch bycatch was dominated by silky sharks (Carcharhinus falciformis). Substantial proportions of dead discards were also observed for other pelagic species, including night sharks (C. signatus) and bigeye thresher sharks (Alopias superciliosus), as well as several coastal species, notably dusky sharks (C. obscurus). Comparison of mean lengths to published estimates of size-at-maturity indicates that, for many species, bycatch in this area is immature. Key words: pelagic longlines, shark bycatch, fisheries.

Introduction The US Atlantic pelagic longline fishery primarily targets swordfish and tuna using monofilament longline gear. The National Marine Fisheries Service (NMFS) has had a mandatory observer program for this fishery since 1992. During 1992–1997, 608 sets of gear were observed in an area bounded by 22°N and 35°N latitude and 71°W and 82°W longitude (Fig. 20.1). Mean yearly observed effort was 2.6% of the reported mean total effort.

Methods and Results A total of 2,649 elasmobranchs, including both pelagic and coastal sharks, were documented in the bycatch by NMFS observers (Table 20.1). Silky sharks (Carcharhinus falciformis, Carcharhinidae) were dominant (34.4% of elasmobranch bycatch), while other pelagic species observed included blue sharks (Prionace glauca, Carcharhinidae; 8.9%), night sharks (C. signatus, Carcharhinidae; 4.6%), oceanic whitetips (C. longimanus, Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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243

35ºN

71ºW

82ºW

22ºN Fig. 20.1 Locations of pelagic longline sets observed off the southeastern United States, 1992–1997.

Carcharhinidae; 3.5%), rays (Dasyatidae and Mobulidae; 2.5%), bigeye thresher (Alopias superciliosus, Alopiidae; 2.2%), and shortfin mako (Isurus oxyrinchus, Lamnidae; 2.1%). Coastal shark species were also observed, notably dusky sharks (C. obscurus, Carcharhinidae; 16.3%). Coastal sharks also made up the majority of a “miscellaneous” category (10.8%), which included nine species and unidentifiable sharks. Elasmobranch bycatch represented 18% of the total longline catch, compared to 48% for targeted catch; the remaining 34% consisted mainly of nontarget teleosts and small numbers of protected species (marine mammals, turtles, and seabirds). Catch status (percentage of animals dead or alive at gear retrieval) varied considerably among species, with silky, dusky, night, scalloped hammerhead (Sphyrna lewini, Sphyrnidae), and bigeye thresher being observed dead on gear retrieval the majority of the time; blue, tiger (Galeocerdo cuvier, Carcharhinidae), oceanic whitetip, sandbar (C. plumbeus, Carcharhinidae), shortfin mako, and rays were most frequently observed alive (Table 20.1). Catch disposition (percentage of animals retained, discarded dead, or released alive) also varied. The proportions retained no doubt are related to the marketability of the species. For example, nearly 60% of the shortfin mako bycatch – a highly marketable species – was kept, but only 0.5% of the less marketable blue shark bycatch was kept. Species frequently discarded dead included silky, dusky, scalloped hammerhead, night, and bigeye thresher sharks. Since many of these species are subject to quota limitations, however, some of the dead discards may represent regulatory discards, particularly those species in the large coastal management group such as silky and dusky sharks.

244

Common name

Scientific name

Species composition (% of total)

Status (% dead)

Disposition % retained

% discarded dead

% released alive

Pelagic sharks Silky Blue Night Oceanic whitetip Bigeye thresher Shortfin mako

Carcharhinus falciformis Prionace glauca C. signatus C. longimanus Alopias superciliosus Isurus oxyrinchus

34.4 8.9 4.6 3.5 2.2 2.1

69.1 13.2 75.8 25.5 58.6 34.5

41.0 0.5 32.9 24.5 8.7 59.2

40.1 18.3 37.5 16.5 48.3 20.4

18.9 81.2 29.6 59.0 43.0 20.4

Coastal sharks Dusky Tiger Scalloped hammerhead Sandbar

C. obscurus Galeocerdo cuvier Sphyrna lewini C. plumbeus

16.3 5.9 5.7 3.1

52.1 2.5 59.2 23.6

27.6 3.3 15.3 35.5

37.1 6.3 50.4 23.0

35.3 90.4 34.3 41.5

Dasyatidae and Mobulidae

2.5 10.8

0.0 –

0.0 –

3.0 –

97.0 –

Others Rays Miscellaneous

Sharks of the Open Ocean

Table 20.1 Species composition, status (condition on gear retrieval), and retained, discarded dead, and released alive percentages observed in elasmobranch bycatch (n
2,649) on pelagic longlines off the southeastern United States, 1992–1997.

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245

Table 20.2 Sex ratio, mean fork length, and reported size-at-maturity for sharks (n
2,649) observed on pelagic longlines off the southeastern United States, 1992–1997.a Common name

Sex ratio (male:female)

Mean fork length (cm)

Reported size-at-maturity (cm)

Reference

Pelagic sharks Silky Blue Night Oceanic whitetip Bigeye thresher Shortfin mako

1:1.3 1:2.8 1:0.8 1:1.2 1:0.8 1:0.5

103 183b 111 110 192b 182

186 183 156 145 172 179

Bonfil et al. (1993) Pratt (1979) Hazin et al. (2000) Lessa et al. (1999) Moreno and Morón (1992) Stevens (1983)

Coastal sharks Dusky Tiger Scalloped hammerhead Sandbar

1:0.8 1:2.1 1:1.8 1:0.8

115 207b 151 145

231 258 139 150

Natanson et al. (1995) Branstetter et al. (1987) Branstetter (1987) Sminkey and Musick (1995)

a Where sources reported a size range for maturity or if size-at-maturity differed between sexes, the minimum size is shown. Where sources reported size as total length, conversions to fork length were made according to Kohler et al. (1995). b Value includes estimated lengths.

Calculation of mean fork lengths was based on actual measurements for most species, but estimated lengths were included in some cases, generally for species that tended to be alive upon gear retrieval. The observed mean fork lengths for silky, dusky, night, and oceanic whitetip were less than reported size-at-maturity (Table 20.2). For blue, shortfin mako, and bigeye thresher sharks, mean lengths were greater than reported size-at-maturity. Interpretation of length data in this study is made difficult by a poor understanding of patterns of longline gear selectivity. “Bite-offs,” or broken leaders, are commonly reported by observers during gear retrieval, suggesting that larger animals, particularly large sharks, may more easily bite through or break the heavy monofilament leaders generally used by this fishery and escape the gear. This potential selectivity would result in a smaller mean observed size. It is possible, therefore, that larger, sexually mature sharks may be more prevalent in the study area than these data indicate. It seems clear, however, that bycatch mortality in this area impacts mostly immature sharks, particularly those of the genus Carcharhinus. Sex ratios were generally close to 1:1 for most pelagic sharks (Table 20.2), with the exception of blue sharks and shortfin makos, which were dominated by females and males, respectively. Blue sharks are commonly encountered in the northern portion of the study area only during the late winter and early spring. Blue shark females grow larger than males; assuming that the gear selectively retains smaller sharks, the dominance of female blue sharks in the bycatch suggests that females are truly dominant in the local population. For shortfin makos, in contrast, observers documented twice as many males as females. Since female makos grow much larger than males, it is unclear whether this sex ratio reflects gear selectivity for the smaller males or actual population gender characteristics. Sexual segregation has been documented in blue sharks (Pratt, 1979), but is less well known for shortfin makos (Casey and Kohler, 1992).

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This study illustrates the kind of information that NMFS observers collect and how it can be used to characterize a fishery’s interaction with elasmobranchs. It also raises concerns by suggesting that, for some species, pelagic longline gear in this area results in substantial bycatch mortality of immature individuals. Examination of additional observer data has allowed more rigorous analyses, providing a clearer perspective on the fisheries biology of elasmobranchs that utilize the pelagic environment (Beerkircher et al., 2002).

Acknowledgments We thank D. Lee and C. Brown of the NMFS Pelagic Observer Program, as well as the observers who collected the data.

References Beerkircher, L. R., Cortés, E. and Shivji, M. (2002) Characteristics of shark bycatch observed on pelagic longlines off the southeastern United States, 1992–2000. Marine Fisheries Review 64(4), 40–49. Bonfil, R., Mena, R. and de Anda, D. (1993) Biological parameters of commercially exploited silky sharks, Carcharhinus falciformis, from the Campeche Bank, Mexico. In: Conservation Biology of Elasmobranchs (ed. S. Branstetter). NOAA Technical Report NMFS 115. NOAA/NMFS, Silver Spring, MD, pp. 73–86. Branstetter, S. (1987) Age, growth, and reproductive biology of the silky shark, Carcharhinus falciformis, and the scalloped hammerhead, Sphyrna lewini, from the northwestern Gulf of Mexico. Environmental Biology of Fishes 19(3), 161–173. Branstetter, S., Musick, J. A. and Colvocoresses, J. A. (1987) A comparison of the age and growth of the tiger shark, Galeocerdo cuvier, from off Virginia and from the northwestern Gulf of Mexico. Fishery Bulletin 85(2), 269–279. Casey, J. G. and Kohler, N. E. (1992) Tagging studies on the shortfin mako shark (Isurus oxyrinchus) in the western North Atlantic. Fishery Bulletin 43, 45–60. Hazin, F. H. V., Lucena, F. M., Souza, T. S. A. L., Boeckman, C. E., Broadhurst, M. K. and Menni, R. C. (2000) Maturation of the night shark, Carcharhinus signatus, in the southwestern equatorial Atlantic Ocean. Bulletin of Marine Science 66(1), 173–185. Kohler, N. E, Casey, J. G. and Turner, P. A. (1995) Length–weight relationships for 13 species of sharks from the western North Atlantic. Fishery Bulletin 93, 412–418. Lessa, R., Santana, F. M. and Peglerani, R. (1999) Age, growth, and stock structure of the oceanic whitetip shark, Carcharhinus longimanus, from the southwestern equatorial Atlantic. Fisheries Research 42, 21–30. Moreno, J. A. and Morón, J. (1992) Reproductive biology of the bigeye thresher shark, Alopias superciliosus (Lowe, 1839). Australian Journal of Marine and Freshwater Research 43, 77–86. Natanson, L. J., Casey, J. G. and Kohler, N. E. (1995) Age and growth estimates for the dusky shark, Carcharhinus obscurus, in the western North Atlantic Ocean. Fishery Bulletin 93, 116–126. Pratt, H. L. (1979) Reproduction in the blue shark, Prionace glauca. Fishery Bulletin 77(2), 445–469. Sminkey, T. R. and Musick, J. A. (1995) Age and growth of the sandbar shark, Carcharhinus plumbeus, before and after population depletion. Copeia 1995(4), 871–883. Stevens, J. D. (1983) Observations on reproduction in the shortfin mako Isurus oxyrinchus. Copeia 1983(1), 126–130.

Chapter 21

Pelagic Shark Fisheries in the Indian Ocean Malcolm J. Smale

Abstract Information on catches of open ocean sharks in the Indian Ocean is limited, but more than 15 species from five families are taken in the region’s fisheries, with blue and silky sharks probably making up the bulk of these catches. Shark catches recorded in the Indian Ocean Tuna Commission database indicate that shark data submissions have improved since the year 2000, but most of the landings are still not identified to species and are grouped as “sharks.” Reported shark catches have generally been increasing since the early 1990s, partly because more countries are submitting records. Yet these represent only part of the true catch, most of which is likely discarded (or saved as fins only) and not logged. South African pelagic shark longline records and shark catches made by the Natal Sharks Board bather protection nets off KwaZulu-Natal are examined to reveal trends in catches. Quantification and validation of commercial shark catches by observer programs are urgently needed to estimate actual catches and effort. Improved data collection will allow for more accurate scientific assessment of catch trends and will enable fishery managers to formulate more effective measures that may lead to sustainable shark fisheries. Unfortunately, progress toward implementation of the Food and Agriculture Organization’s Plan of Action for Sharks in the Indian Ocean region has been slow. Given the probable decline in shark populations over the last few decades, it is suggested that the feasibility of open ocean marine reserves be investigated with the aim of contributing toward greater marine ecosystem protection in the Indian Ocean. Key words: Indian Ocean, Lamnidae, Alopiidae, Carcharhinidae, marine protected areas, shark management, shark fisheries.

Introduction Fisheries in the Indian Ocean include artisanal, recreational, and commercial fisheries, and all exert significant pressure on shark populations. At least 23 countries have coastlines abutting the Indian Ocean, including three of the top five elasmobranch-fishing nations in the world. In 2002, 29 countries reported elasmobranch landings from the Indian Ocean totaling 257,908 metric tons (t), or almost 32% of the global landings for that year (Food and Agriculture Organization, FAO, 2003). India led the landings with Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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67,358 t, followed by Pakistan (49,904 t), Indonesia (32,880 t), Sri Lanka (25,340 t), Spain (16,002 t), Maldives (11,498), and Thailand (10,321 t). These statistics include catches by all gears and in all habitats (pelagic as well as demersal), but are not species specific. Tuna fisheries use longlines, purse seines, and even pelagic drift nets (although the latter practice has probably declined since the international moratorium imposed in the early 1990s). They are known to have a large bycatch of sharks and are the focus of this chapter. Catch records compiled by the Indian Ocean Tuna Commission (IOTC) are presented to determine which shark species are caught and to investigate trends in catches in the region. Recent information from the South African pelagic shark-fishing fleet is also presented, and catch trends for open ocean sharks taken by the Natal Sharks Board bather protection nets (NSB nets) are discussed in relation to catches of pelagic sharks in the Indian Ocean.

Shark catches Record keeping of shark catches by fishery vessels operating in the Indian Ocean is poor, and catches are rarely identified to the species level, other than during some research surveys. Thus accurate quantitative information on the shark species caught in the Indian Ocean is generally lacking (Barnett, 1997a, b; Cooke, 1997; Marshall, 1997a, b, c, d; Smale, 1997; Sousa et al., 1997). Information from some areas, such as the Maldives, is better, because research surveys have identified shark species and estimated total catches (Anderson and Waheed, 1999; Anderson and Hafiz, 2002). Catch data reported to the IOTC generally exclude sharks, but when they are included, data reliability is questionable because of the lack of observers. Most sharks are finned and the carcasses dumped at sea, and the sharks caught are often not recorded. As a result, shark records underestimate total shark catches (Bonfil, 2002; M. Herrera, IOTC, personal communication, 2004). The creation of an IOTC Working Party on Bycatch in 2002 and recent efforts to improve species-specific reporting of non-tuna catches should help close data gaps that still exist (IOTC, 2005). Nonetheless, IOTC data have shown a rapid increase in shark catch over the last two decades, particularly in the 1990s (Fig. 21.1(a)). These data are from a variety of sources, including country reports and submissions to the FAO. One of the reasons for the increase is the greater number of countries for which improved information is available (Fig. 21.1(b)), but there may also be an increase in fishing effort for sharks in the western Indian Ocean (WIO; FAO fishing area 51) compared to the eastern Indian Ocean (EIO; FAO fishing area 57). Furthermore, some countries have started to target sharks in recent years, although given the limits of the data (species lumping, unrecorded catches, lack of effort data, and absence of observers), caution must be exercised in interpreting these data, particularly because total catch and total effort remain unknown. Anderson and Ahmed (1993) and Anderson and Hafiz (2002) described the shark fishery off the Maldives and noted that export demand for dried fins has driven a local pelagic longline fishery for oceanic sharks. In addition, commercial high-seas tuna fleets operated by European and Far East nations take poorly documented numbers of these sharks as bycatch. Japanese statistics for the Indian Ocean record 25 species in the longline catch and, although data are incomplete, more than two-thirds of the catch is discarded because of its low value compared to tunas (Taniuchi, 1990). Japanese elasmobranch catches are declining steadily,

Pelagic Shark Fisheries in the Indian Ocean

249

50,000

Metric tons

40,000

30,000

FAO fishing area 51 WIO FAO fishing area 57 EIO

20,000

10,000

0 1960

1970

1980

1990

2000

1990

2000

Years (a)

Number countries' data

70 60

FAO fishing area 51 WIO

50

FAO fishing area 57 EIO

40 30 20 10 0 1960

1970

1980 Years (b)

Fig. 21.1 (a) Total annual catch of sharks in the WIO (FAO fishing area 51) and the EIO (FAO fishing area 57) as recorded in the IOTC database. (b) Number of countries for which annual catch records are available in the IOTC database.

and sharks taken by distant-water longliners are used mainly for fins, although shortfin makos are used more fully (Nakano, 1999). The Taiwanese tuna longline fishery in the Indian Ocean was initiated in 1963 (Hsu and Liu, 1990; although IOTC data suggest that it started in 1954), and most of its effort is focused in two areas: 10°S to 40°S and 5°S to 10°N. Although the target areas changed seasonally, effort reached 300 million hooks in 1988 (Hsu and Liu, 1990). Large-scale pelagic drift-net fisheries were initiated in 1983, and the number of boats increased to 149 in the 1987–1988 fishing season. “Shark” catches

250

Sharks of the Open Ocean

made up 23.8% by number and 29.6% by weight of pelagic drift-net catches in 1986–1987, and 0.5% by number and 2.1% by weight in 1987–1988. Whether this drop was a consequence of rapid decline in shark populations, or changes in fishing method or reporting levels, is unknown. The moratorium on pelagic drift-net fishing imposed in the early 1990s was widely adopted internationally, although levels of compliance are unknown. Sharks on the Seychelles plateau and nearby banks showed signs of overexploitation as early as the 1950s according to Travis (1990), and prompted more distant waters to be exploited. Although shark meat is of low commercial value in the Seychelles, open ocean and inshore species are caught for their fins and for artisanal crafts (Nageon de Lestang, 1999). India and Sri Lanka are major elasmobranch-fishing nations in the Indian Ocean. Although both countries have long shark-fishing histories, the recent increased popularity of shark meat and, in particular, the high prices paid for fins for export have driven targeted shark fisheries using a variety of gear (Hanfee, 1999; Joseph, 1999). The catch composition in these fisheries is poorly documented; some of the pelagic sharks taken include blue sharks (Prionace glauca, Carcharhinidae), threshers (Alopias spp., Alopiidae), and makos (Isurus spp., Lamnidae). The rapid increase in tuna catches in the Indian Ocean to over 700,000 t in 1999 makes it one of the world’s largest tuna fisheries, conducted mainly by European Union, Japanese, and Taiwanese fleets (Anonymous, 2001, p. 59). The range of shark bycatch recorded in the IOTC database was 7,043–13,871 t/year during the 1970s, 5,921–17,784 t in the 1980s, 16,694–75,250 t in the 1990s, and 61,202–71,638 t from 2000 to 2002. The increase is believed to be a result of more complete reporting of the catches, rather than any other factor, and the data are still incomplete (M. Herrera, IOTC, personal communication, 2004). Of the total of 780,486 t of sharks in the database from 1970 to 2002, less than 10% is identified to species and the remainder is recorded as “unidentified sharks.” Examination of the improved data from 2000 to 2002 indicates that a greater proportion of the catch (68,140 t) is identified, although 64% is still recorded as “sharks” (Fig. 21.2). An annual

Blue sharks 19% Silky sharks 9%

Oceanic whitetip sharks 2% Requiem sharks 2% Sharks 64%

Hammerhead sharks 1% Mackerel sharks 1% Shortfin mako sharks 1%

Thresher sharks 1%

Fig. 21.2 Proportions of all sharks reported in the IOTC database for the period 2000–2002 (WIO and EIO combined).

Pelagic Shark Fisheries in the Indian Ocean

251

average of 33,219 t of unidentified “sharks” were taken in 2000–2002 in the WIO, whereas 9,085 t were recorded from the EIO during this period (Fig. 21.3). Pelagic shark landings by licensed South African longliners in both Atlantic and Indian Ocean grounds have increased substantially from the early 1990s (Fig. 21.4). The average annual catch of makos, the principal pelagic shark recorded, doubled from 64.3 t in the 1990s to at least 133 t in the 2000s (the 2004 data include landings from January through 10,000 Annual average mass (t)

9,000

33,219 t

WIO

8,000

EIO

7,000 6,000 5,000 4,000 3,000 2,000 1,000 Thresher sharks

Shortfin mako sharks

Silky sharks

Sharks

Mackerel sharks

Requiem sharks

Oceanic whitetip sharks

Blue sharks

Hammerhead sharks

0

Fig. 21.3 Annual average mass of sharks reported for 2000–2002 for the WIO and EIO. Unidentified sharks from the WIO averaged 33,219 t/year for this period.

300

Metric tons

250 Mako shark Blue shark

200 150 100 50

2004

2003

2002

2001

2000

1999

1998

1997

1996

1995

1994

1993

1992

0

Years Fig. 21.4 Annual reported catches of the two principal shark species taken by the South African pelagic longline fishery (Indian and Atlantic Ocean fishing grounds). The 2004 catch includes only the months January through May.

252

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May). The large fluctuations are a result of switching target species and are partly market driven (S. Pheeha, Marine and Coastal Management, personal communication, 2004). Small quantities of other pelagic species, such as thresher sharks, were also taken. Another important shark fishery in South Africa is the inshore bather protection nets off KwaZuluNatal operated by the NSB. These nets caught an annual average of 1,228 sharks after 1970, mainly inshore species (Cliff and Dudley, 1992; Dudley and Simpfendorfer, 2006). Although detailed information on catches of sharks in the Indian Ocean is limited, there is evidence that elasmobranchs are under pressure. Anderson et al. (1998) recorded a decrease by a factor of about 10 in shark numbers at Chagos in the northern Indian Ocean in 1996 compared to the 1970s. These sharks were largely reef associated, and they included the silvertip (Carcharhinus albimarginatus, Carcharhinidae), which is commonly taken on lines, suggesting that sharks have been subject to fishing effort great enough to reduce populations in at least some localities to well below their former levels. More recently, Spalding (2003) suggested that there might have been a partial recovery of reef sharks at Chagos as a result of management efforts, although he notes the need for further surveys to improve assessments.

Commonly caught species Lamnidae The white shark, Carcharodon carcharias, is common in South African waters, especially near seal colonies, and is caught in NSB nets (Cliff et al., 1989). Large adults have occasionally been recorded in the tropical Indian Ocean when tangled in gill nets (Cliff et al., 2000; Zuffa et al., 2002). A first estimate of population size off the South African coast between Struis Bay and Richards Bay (approximately 1,375 km) was 1,279 sharks (95% confidence limits, 839–1,843 sharks) based on 73 tagged sharks (Cliff et al., 1996). The annual catch of white sharks in NSB nets between 1978 and 2003 averaged 35.8 sharks (standard deviation
13.5). Catch rates did not show a significant decline, although there was a significant decrease in mean length of females over this time period (Dudley and Simpfendorfer, 2006). The shortfin mako, Isurus oxyrinchus, is caught widely throughout the Indian Ocean, including the waters of India (Hanfee, 1999), Western Australia (Simpfendorfer, 1999), and South Africa (Smale, 1997). A total of 3,790 t of shortfin mako are recorded in the IOTC database between 1970 and 2002, more than 90% of which was taken in the WIO. Pregnant females were among the shortfin makos caught in NSB nets, suggesting that pupping may occur in the region in late spring (Cliff et al., 1990). Juveniles and adults are caught by sport, pelagic longline, and research line fishing off the southern coast of South Africa (M. Smale, unpublished data) and off Namibia (Compagno et al., 1991). Annual catches of this species in NSB nets between 1978 and 2003 were low (mean
13.4, standard deviation
4.5 sharks), and there was no significant trend in catch rate or size of sharks caught over the time period (Dudley and Simpfendorfer, 2006). Although the longfin mako, I. paucus, is sometimes confused with the shortfin mako, landings of longfin total 86.9 t in the IOTC database between 1993 and 2002. During

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2000–2002, 10 t were recorded from the WIO, but none from the EIO. The longfin mako is a poorly known tropical oceanic species and has been recorded off the Comoro Islands (M. Smale, unpublished data), Sri Lanka (Joseph, 1999), and (in part as I. oxyrinchus) Madagascar (Fourmanoir, 1961). Porbeagle sharks, Lamna nasus, are taken by tuna longliners in temperate waters of the Indian Ocean (Compagno, 2001), but are poorly recorded in commercial fishing logs. The size of the catch is unknown and there is only one record of 4.5 t in the IOTC database (in 1999).

Alopiidae All three species of thresher sharks occur in the Indian Ocean and are taken by commercial, sport, and occasionally artisanal fisheries (Fourmanoir, 1961; Gubanov, 1972, 1979; Bass et al., 1975). Threshers total 3,294 t in the IOTC records (recorded from 1994 to 2002), and they made up 1% of Indian Ocean catches in 2000–2002 (Fig. 21.2); they were more dominant in the EIO (Fig. 21.3). Spalding (2003) estimated that almost 2,000 thresher sharks were taken off Chagos by longliners as bycatch in 1998–1999, suggesting that this catch rate may not be sustainable.

Carcharhinidae A large number of carcharhinids are taken in open-water fisheries for tunas and other pelagic teleosts. The shark species caught depend on the fishing locality and depth (Anderson and Waheed, 1999; Joseph, 1999). The silvertip, frequently taken by longline and artisanal fisheries in the Indian Ocean, is common near islands and offshore banks (Wheeler, 1953; Fourmanoir, 1961; Bass et al., 1973; Anderson and Waheed, 1999; M. Smale, unpublished data). Sometimes seen near coral reefs by divers, juveniles are found around atolls, whereas large individuals are caught offshore by longlines (Anderson and Ahmed, 1993). Off Chagos, this species has been markedly reduced by fishing (Anderson et al., 1998), and this has probably happened throughout its range. The silky shark, Carcharhinus falciformis, is distributed through the Indian Ocean, from the east coast of Africa, Madagascar, and the Red Sea, along the Arabian Peninsula, and east to India and Sri Lanka; its distribution in the EIO is less clear (Fourmanoir, 1961; Bass et al., 1973; Compagno, 1984). Off the Maldives it is the most important pelagic shark taken offshore, composing 70–80% by numbers caught (Anderson and Waheed, 1999; Anderson and Hafiz, 2002). It is the dominant shark in both the coastal and offshore fisheries of Sri Lanka (Joseph, 1999). IOTC data indicate Sri Lankan records of 7,260, 10,989, 4,166, and 2,991 t annually from 1999 to 2002, respectively; the recent decline may indicate overexploitation of the stock. Thought to be one of the more common offshore carcharhinids, it is found near the surface in open water from 50 to 3,000 m and has been recorded on deep longlines at 100–199 m and 400–499 m (Forster et al., 1970; Bass et al., 1973). More than 99% of the 25,434 t of silky sharks caught between 1997 and 2002 in the Indian Ocean were taken in the EIO (Fig. 21.3), and silkys made up 9% of the IOTC records for 2000–2002 (Fig. 21.2).

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The oceanic whitetip, C. longimanus, is probably the most oceanic shark of the Carcharhinidae. It has been described as one of the most abundant sharks in the Mauritius/ Seychelles area (Wheeler, 1953; Bass, 1970; Bass et al., 1973; Prado and Drew, 1991), although its current status there is uncertain. It is commonly caught off the Maldives by pelagic longliners and as tuna bycatch (Anderson and Hafiz, 2002). Smaller individuals are caught in shallower water, and this shark may exhibit sexual and geographic separation (Anderson and Ahmed, 1993). Landings total 5,630 t in IOTC records between 1997 and 2002. In the period 2000–2002, the whitetip made up 2% of the IOTC records (Fig. 21.2), and was apparently more dominant in identified catches from the EIO (1,610 t) than the WIO (5 t) (Fig. 21.3). The blue shark has a global distribution (Compagno, 1984) and is common off the southern African Atlantic coast and in the Indian Ocean (Bass et al., 1975; Gubanov and Grigor’yev, 1975; Compagno et al., 1991; Joseph, 1999); it is frequently recorded in longline catches off South Africa (Smale, 1997; Japp, 1999). They may move long distances: Of 10 blue sharks tagged by the author during research cruises off South Africa, one female released at Danger Point on 28 January 1997 (34º38S, 19º18E) was recaptured in the central Atlantic (00º05S, 1º06E) on 1 August 1998, more than 4,300 km away. It had grown from 177 to 195 cm total length (M. Smale, unpublished data). Gubanov (1979) recorded mature females in the equatorial Indian Ocean from 180 to 352 cm, but no blue sharks smaller than 130 cm were taken. The total catch of blue shark recorded by the IOTC is 43,997 t from 1994 to 2002. Between 2000 and 2002, it was the principal identified shark in the IOTC database at 19% (Fig. 21.2). Its annual catch averaged 9,496 t in the WIO compared to 3,349 t in the EIO from 2000 to 2002 (Fig. 21.3). Spalding (2003) estimated that more than 3,000 individuals were removed from Chagos waters in 1 year, giving credence to the contention that this shark is under considerable pressure from pelagic fisheries.

Management and conservation The difficulties of managing highly migratory species that straddle high seas and the exclusive economic zones (EEZ) of coastal nations have been outlined by FAO (1994). Because of declining catches and the need to manage resources that fall outside the control of individual countries, the IOTC is working to improve the management of important commercial species. Despite such agreements, there is a large shark bycatch in Indian Ocean fisheries and there is a lack of motivation for their conservation by several significant fishing nations (Shotton, 1999; Bonfil, 2002). Baum et al. (2003) suggested that several shark populations have declined by over 75% in the past 15 years in the Northwest Atlantic. In the Indian Ocean, there is a paucity of reliable data on shark catches, bycatch, and effort, which limits our ability to assess historical changes in shark catches in this ocean. The situation is exacerbated by the fact that many countries bordering the Indian Ocean are developing African and Asian states that have limited capacity to assess, manage, or control access to their EEZs, which often include areas of open ocean (Barnett, 1997a). An exception is Australia, which has implemented advanced management protocols for its fisheries, including for sharks (Simpfendorfer, 1999; Stevens, 2002).

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Piracy of resources within EEZs by foreign vessels is widely reported by coastal communities, particularly off Africa. Such illegal fishing is widespread and poorly documented, and its impact is likely to be highly detrimental to shark populations. There is growing awareness of these management and enforcement problems regarding shark fisheries. For example, IOTC Resolution 05/05 of 2005 proposes, among other things, the full utilization of targeted sharks, the banning of all finning, annual reporting of shark catches (including compiling available historical data), and, if the fishery is not shark directed, live release of juveniles and pregnant females (see www.iotc.org). Until observer programs are initiated throughout the area, knowledge of the catch will remain poor, fishing effort will remain unknown, and it will be impossible to assess changes in catch rates, which will prevent the development of management plans. Adequate management plans are urgently needed because the life-history traits of chondrichthyans severely limit their stock rebuilding potential (Smith et al., 1998, 2008; Au et al., 2008; Cortés, 2008). Furthermore, because of the difficulty of monitoring and managing open ocean fisheries, there is a strong case for investigating the feasibility of open ocean protected areas to provide refuge for members of the pelagic ecosystem. However, Baum et al. (2003) warned that such an approach needs to be investigated thoroughly to avoid merely displacing, and possibly increasing, fishing effort to sensitive areas. As noted by Compagno (1990), the idea of worldwide management of chondrichthyan fisheries may be utopian – indeed, there has been little improvement over the past decade, even though there have been efforts to improve data collection (although much of the data are of dubious quality) and International Plans of Action have been adopted by some nations. Until the neglect of shark management is rectified internationally, the prognosis for shark populations (and other fishes) of the open ocean is poor at best. Unfortunately, the widespread concern that has been voiced about the detrimental ecosystem effects of unsustainable levels of shark fishing (Stevens et al., 2000) has yet to be translated into sustainable fishing agreements.

Acknowledgments I thank Dr. Merry Camhi for inviting me to contribute to this volume, and the Port Elizabeth Museum and National Research Foundation for financial support. Mr. S. Pheeha kindly sent me data on South African pelagic shark catches held by Marine and Coastal Management. I gratefully acknowledge access to data held by the Indian Ocean Tuna Commission, and Miguel Herrera for facilitating this process and commenting on a draft of this chapter. Comments by two anonymous reviewers improved this contribution. The IOTC data used in this chapter are from a report to the Working Party on Data Collection and Statistics, and may be found at www.iotc.org.

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Anderson, R. C. and Hafiz, A. (2002) Elasmobranch fisheries in the Maldives. In: Elasmobranch Biodiversity, Conservation and Management (eds. S. L. Fowler, T. M. Reed and F. A. Dipper). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 114–121. Anderson, R. C. and Waheed, Z. (1999) Management of shark fisheries in the Maldives. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 367–401. Anderson, R. C., Sheppard, C., Spaldin, C. and Crosby, R. (1998) Shortage of sharks at Chagos. Shark News. The Newsletter of the IUCN Shark Specialist Group 10, 1–3. Anonymous (2001) Report of the Fifth Session of the Indian Ocean Tuna Commission, 11–15 December 2000. Document IOTC/S/05/00/R[E]. IOTC, Victoria, Seychelles, 70 pp. Au, D. W., Smith, S. E. and Show, C. (2008) Shark productivity and reproductive protection, and a comparison with teleosts. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Barnett, R. (1997a) Shark fisheries and trade in East and Southern Africa. In: The Trade in Sharks and Shark Products in the Western Indian and Southeast Atlantic Oceans (eds. N. T. Marshall and R. Barnett). TRAFFIC East/Southern Africa, Nairobi, Kenya, pp. 5–12. Barnett, R. (1997b) The shark trade in mainland Tanzania and Zanzibar. In: The Trade in Sharks and Shark Products in the Western Indian and Southeast Atlantic Oceans (eds. N. T. Marshall and R. Barnett). TRAFFIC East/Southern Africa, Nairobi, Kenya, pp. 39–66. Bass, A. J. (1970) Report on a Shark Survey at St. Brandon during November 1970. Unpublished report, Oceanographic Research Institute, Durban, South Africa, 20 pp. Bass, A. J., D’Aubrey, J. D. and Kistnasamy, N. (1973) Sharks of the East Coast of Southern Africa. I. The Genus Carcharhinus (Carcharhinidae). Investigational Report No. 33. Oceanographic Research Institute, Durban, South Africa, 168 pp. Bass, A. J., D’Aubrey, J. D. and Kistnasamy, N. (1975) Sharks of the East Coast of Southern Africa. III. The Families Carcharhinidae (excluding Mustelus and Carcharhinus) and Sphyrnidae. Investigational Report No. 38. Oceanographic Research Institute, Durban, South Africa, 100 pp. Baum, J. K., Myers, R. A., Kehler, D. G., Worm, B., Harley, S. J. and Doherty, P. A. (2003) Collapse and conservation of shark populations in the northwest Atlantic. Science 299, 389–392. Bonfil, R. (2002) Trends and patterns in world and Asian elasmobranch fisheries. In: Elasmobranch Biodiversity, Conservation and Management (eds. S. L. Fowler, T. M. Reed and F. A. Dipper). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 15–24. Cliff, G. and Dudley, S. F. J. (1992) Protection against shark attack in South Africa, 1952–1990. In: Sharks: Biology and Fisheries (ed. J. G. Pepperell). Australian Journal of Marine and Freshwater Research 43(special volume), 263–272. Cliff, G., Dudley, S. F. J. and Davis, B. (1989) Sharks caught in the protective gill nets off Natal, South Africa. 2. The great white shark Carcharodon carcharias (Linnaeus). South African Journal of Marine Science 8, 131–144. Cliff, G., Dudley, S. F. J. and Davis, B. (1990) Sharks caught in the protective gill nets off Natal, South Africa. 3. The shortfin mako shark Isurus oxyrinchus (Rafinesque). South African Journal of Marine Science 9, 115–126. Cliff, G., van der Elst, R. P., Govender, A., Witthuhn, T. K. and Bullen, E. M. (1996) First estimates of mortality and population size of white sharks on the South African coast. In: Great White Sharks: The Biology of Carcharodon carcharias (eds. A. P. Klimley and D. G. Ainley). Academic Press, San Diego, CA, pp. 393–400. Cliff, G., Compagno, L. J. V., Smale, M. J., van der Elst, R. P. and Wintner, S. P. (2000) First records of white sharks, Carcharodon carcharias, from Mauritius, Zanzibar, Madagascar and Kenya. South African Journal of Science 96, 365–367.

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Compagno, L. J. V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Parts 1 and 2. FAO Fisheries Synopsis No. 125. FAO, Rome, Italy, 655 pp. Compagno, L. J. V. (1990) Shark exploitation and conservation. In: Elasmobranchs As Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries (eds. H. L. Pratt, S. H. Gruber and T. Taniuchi). NOAA Technical Report NMFS 90. NOAA/NMFS, Silver Spring, MD, pp. 391–414. Compagno, L. J. V. (2001) FAO Species Catalogue for Fishery Purposes. No. 1. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Vol. 2. Bullhead, Mackerel and Carpet Sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO, Rome, Italy, 269 pp. Compagno, L. J. V., Ebert, D. A. and Cowley, P. D. (1991) Distribution of offshore demersal cartilaginous fish (class Chondrichthyes) off the west coast of southern Africa, with notes on their systematics. South African Journal of Marine Science 11, 43–139. Cooke, A. J. (1997) Survey of elasmobranch fisheries and trade in Madagascar. In: The Trade in Sharks and Shark Products in the Western Indian and Southeast Atlantic Oceans (eds. N. T. Marshall and R. Barnett). TRAFFIC East/Southern Africa, Nairobi, Kenya, pp. 101–130. Cortés, E. (2008) Comparative life history and demography of pelagic sharks. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Dudley, S. F. J. and Simpfendorfer, C. A. (2006) Population status of 14 shark species caught in the protective gillnets off KwaZulu-Natal beaches, South Africa, 1978–2003. Marine and Freshwater Research 57(2), 225–240. FAO (1994) World Review of Highly Migratory Species and Straddling Stocks. FAO Fisheries Technical Paper No. 337. FAO, Rome, Italy, 70 pp. FAO (2003) FISHSTAT Plus, Version 2.3. Capture Production Database, 1970–2002, and Commodities Trade and Production Database, 1976–2002. FAO, Rome, Italy. Forster, G. R., Badcock, J. R., Longbottom, M. R., Merrett, N. R. and Thomson, K. S. (1970) Results of the Royal Society Indian Ocean deep slope fishing expedition, 1969. Proceedings of the Royal Society of London, Series B 175, 367–404. Fourmanoir, P. (1961) Requins de la cote ouest de Madagascar. Mémoires de l’Institute Scientifique de Madagascar, Serie F 4, 3–81. Gubanov, Ye. P. (1972) On the biology of the thresher shark [Alopias vulpinus (Bonnaterre)] in the northwest Indian Ocean. Journal of Ichthyology 12, 591–600. Gubanov, Ye. P. (1979) The reproduction of some species of pelagic sharks from the equatorial zone of the Indian Ocean. Journal of Ichthyology 18, 781–792. Gubanov, Ye. P. and Grigor’yev, V. (1975) Observations on the distribution and biology of the blue shark, Prionace glauca (Carcharhinidae) of the Indian Ocean. Journal of Ichthyology 15, 37–43. Hanfee, F. (1999) Management of shark fisheries in two Indian coastal states: Tamil Nadu and Kerala. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 316–338. Hsu, C.-C. and Liu, H.-S. (1990) Taiwanese Longline and Gillnet Fisheries in the Indian Ocean. Expert Consultation on Stock Assessment of Tunas in the Indian Ocean, Bangkok, Thailand, 2–6 July 1990, FAO/IPTP/TWS/90/54. FAO, Rome, Italy, 10 pp. IOTC (2005) Report of the First Session of the IOTC Working Party on Bycatch, Phuket, Thailand, 20 July 2005. Document IOTC-2005-WPBy-R[EN]. IOTC, Victoria, Seychelles, 16 pp. Japp, D. W. (1999) Management of elasmobranch fisheries in South Africa. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 199–217.

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Joseph, L. (1999) Management of shark fisheries in Sri Lanka. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 339–366. Marshall, N. T. (1997a) The Seychelles shark fishery. In: The Trade in Sharks and Shark Products in the Western Indian and Southeast Atlantic Oceans (eds. N. T. Marshall and R. Barnett). TRAFFIC East/Southern Africa, Nairobi, Kenya, pp. 13–18. Marshall, N. T. (1997b) Trade in sharks and shark products in Eritrea. In: The Trade in Sharks and Shark Products in the Western Indian and Southeast Atlantic Oceans (eds. N. T. Marshall and R. Barnett). TRAFFIC East/Southern Africa, Nairobi, Kenya, pp. 19–23. Marshall, N. T. (1997c) The Somali shark fishery in the Gulf of Aden and the western Indian Ocean. In: The Trade in Sharks and Shark Products in the Western Indian and Southeast Atlantic Oceans (eds. N. T. Marshall and R. Barnett). TRAFFIC East/Southern Africa, Nairobi, Kenya, pp. 24–30. Marshall, N. T. (1997d) Trade in sharks and shark products in Kenyan waters. In: The Trade in Sharks and Shark Products in the Western Indian and Southeast Atlantic Oceans (eds. N. T. Marshall and R. Barnett). TRAFFIC East/Southern Africa, Nairobi, Kenya, pp. 31–38. Nageon de Lestang, J. (1999) Management of shark fisheries in Seychelles. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 285–307. Nakano, H. (1999) Fishery management of sharks in Japan. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/2. FAO, Rome, Italy, pp. 552–579. Prado, J. and Drew, S. (1991) Trials and Developments in Small Scale Shark Fishing Carried Out by FAO, 1978–1990. FAO Fisheries Circular No. 840. FAO, Rome, Italy, 68 pp. Shotton, R. (1999) Species identification practices of countries reporting landings of chondrichthyan fisheries in the FAO nominal catches and landings data base. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/2. FAO, Rome, Italy, pp. 904–920. Simpfendorfer, C. (1999) Management of shark fisheries in Western Australia. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 425–455. Smale, M. J. (1997) Trade in sharks and shark products in South Africa. In: The Trade in Sharks and Shark Products in the Western Indian and Southeast Atlantic Oceans (eds. N. T. Marshall and R. Barnett). TRAFFIC East/Southern Africa, Nairobi, Kenya, pp. 80–100. Smith, S. E., Au, D. W. and Show, C. (1998) Intrinsic rebound potential of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678. Smith, S. E., Au, D. W. and Show, C. (2008) Intrinsic rates of increase in pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Sousa, M. I., Marshall, N. T. and Smale, M. J. (1997) The shark trade in Mozambique. In: The Trade in Sharks and Shark Products in the Western Indian and Southeast Atlantic Oceans (eds. N. T. Marshall and R. Barnett). TRAFFIC East/Southern Africa, Nairobi, Kenya, pp. 67–79. Spalding, M. (2003) Partial recovery of reef sharks in Chagos waters. Shark News. The Newsletter of the IUCN Shark Specialist Group 15, 12–13. Stevens, J. (2002) A review of Australian elasmobranch fisheries. In: Elasmobranch Biodiversity, Conservation and Management (eds. S. L. Fowler, T. M. Reed and F. A. Dipper). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 122–126. Stevens, J. D., Bonfil, R., Dulvy, N. K. and Walker, P. A. (2000) The effects of fishing on sharks, rays and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57, 476–494.

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Taniuchi, T. (1990) The role of elasmobranchs in Japanese fisheries. In: Elasmobranchs As Living Resources: Advances in the Biology, Ecology, Systematics and the Status of the Fisheries (eds. H. L. Pratt, S. H. Gruber and T. Taniuchi). NOAA Technical Report NMFS 90. NOAA/NMFS, Silver Spring, MD, pp. 415–426. Travis, W. (1990) Beyond the Reefs and Sharks for Sale. Adventures in the Seychelles. Arrow Books Ltd., London, UK. Wheeler, J. G. F. (1953) Report on the Mauritius–Seychelles Fisheries Survey 1948–49. Part I. The Bottom Fishes of Economic Importance. Fishery Publications of the Colonial Office No. 3. London, 57 pp. Zuffa, M., Van Grevelynghe, G., De Maddalena, A. and Storai, T. (2002) Records of the white shark, Cacharodon carcharias (Linnaeus, 1758), from the western Indian Ocean. South African Journal of Science 98, 347–349.

Chapter 22

Case Study: The Bycatch of Pelagic Sharks in Australia’s Tuna Longline Fisheries John D. Stevens and Sally E. Wayte

Abstract Logbook and observer data from tuna longliners fishing in Australian waters were analyzed for the period 1991–1996, with most of the data from Japanese vessels. Sixteen species (or species groups) of sharks were recorded; 85% of the shark catch was blue shark, 6% was porbeagle, and 3% was shortfin mako. Japanese longliners caught an average of 1,800 metric tons (t) of blue shark, 167 t of mako, and 139 t of porbeagle each fishing season in Australian waters. Blue shark catch rates varied with latitude on the east coast, from about 1.3 sharks per 1,000 hooks at 10–30°S to about 7.7 per 1,000 hooks at 40–50°S. The size of blue sharks in the catch decreased toward the south on the east coast, and a greater proportion of females were caught to the south. No clear latitudinal trend in catch rates or size of shortfin mako was evident, although more females were caught to the north. Porbeagles were caught mainly south of 40°S and were mostly 1-year-old fish. Catch rates of porbeagles recorded by observers on Japanese vessels increased from 1992 to 1996, but probably reflect better identification of this species. There was no consistent decline in catch rates of blue sharks taken by Japanese vessels fishing through the May to July season at 40–50°S on the east coast of Australia. Although current blue shark catch rates by the domestic longline fleet are four to five times lower than those from the observed Japanese fishery of a decade earlier, the cause of the decline awaits further exploration of the data. Key words: bycatch, tuna longline fisheries, catch rates, blue shark, shortfin mako, porbeagle, Prionace glauca, Isurus oxyrinchus, Lamna nasus, Australia, longlining.

Introduction Japanese longliners have fished in Australian waters since the 1960s, initially targeting albacore (Thunnus alalunga, Scombridae) for the canning market and then switching to highquality tunas with development of the sashimi market. With the declaration of the Australian Fishing Zone in 1979, activities of Japanese vessels were progressively restricted to preserve resources for local fisheries. Since 1997, the Japanese have been excluded from Australian waters because of disputes over the southern bluefin tuna (Thunnus maccoyii, Scombridae) Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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stock assessment and allowable catch. Ward (1996) provided a comprehensive history of Japanese longlining in Australian waters. Australian domestic longliners have fished since the 1950s, but their effort expanded rapidly in the 1980s and 1990s, so that current effort is about equivalent to that of the latter stages of the Japanese fleet. This case study presents data on the main species of pelagic sharks taken as bycatch in tuna longline fisheries in Australian waters. Logbook and observer data from Japanese and domestic tuna longliners fishing from 1991 to 1996 were analyzed, but most of the data are from the Japanese fleet. During these 5 years, Japanese vessels set 78 million hooks, with 80% of the effort being in waters south of 30°S.

Species composition From 1992 to 1996, 44,306 sharks were recorded by observers on Japanese longline vessels fishing in Australian waters. This represents 11% of the shark catch recorded in the Japanese logbook data. The species composition of these sharks from observer data is shown in Table 22.1. About 85% of the catch was blue shark (Prionace glauca, Carcharhinidae); porbeagle (Lamna nasus, Lamnidae) and shortfin mako (Isurus oxyrinchus, Lamnidae) make up the next largest component (although in much smaller numbers). Each of the remaining species was less than 1%, with the exception of the small crocodile shark (Pseudocarcharias kamoharai, Lamnidae). No silky sharks (Carcharhinus falciformis, Carcharhinidae) were recorded in either the logbook or the observer data; however, this reflects an identification problem, as they were certainly taken. It is likely that sharks recorded as “bronze whaler” (Carcharhinus spp., Carcharhinidae) in both logbook and observer data were mostly silky sharks, certainly those taken north of about 32°S. Blue sharks dominated the shark bycatch, occurring in 85% of observed sets. They were more abundant in temperate waters, and it should be noted that 83% of observed fishing effort was south of 30°S.

Table 22.1 Species composition (by number) of sharks taken by Japanese longline vessels fishing in Australian waters from 1992 to 1996, based on observer data. Observer name

Scientific name

Blue whaler Porbeagle Shortfin mako Crocodile Dusky Oceanic whitetip Bigeye thresher School Bronze whaler Velvet dogfish Common thresher Dogfish Hammerhead Tiger Pelagic thresher Longfin mako

Prionace glauca Lamna nasus Isurus oxyrinchus Pseudocarcharias kamoharai Carcharhinus obscurus Carcharhinus longimanus Alopias superciliosus Galeorhinus galeus Carcharhinus spp. Zameus squamulosus Alopias vulpinus Squalidae Sphyrna spp. Galeocerdo cuvier Alopias pelagicus Isurus paucus

% composition 84.7 5.5 3.3 2.1 0.7 0.6 0.6 0.5 0.5 0.5 0.4 0.3 0.1 0.1
0.1
0.1

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Catch rates and catch Figure 22.1 shows the distribution of fishing effort for the east coast (east of 140°E) and west coast (west of 120°E) of Australia. Catch rates (number of sharks per 1,000 hooks) of blue sharks derived from logbook and observer data for Japanese longliners were compared for the period 1992–1996, and were examined by latitudinal bands because blue shark abundance can vary with latitude (Stevens, 1992). Blue shark catch rates showed a general increasing trend with increasing latitude (Table 22.2). The highest catch rates on the east coast were in the 40–50°S latitude band and on the west coast in the 30°S region. More limited logbook data from domestic longliners showed a similar trend on the east coast; few data were available for the west coast.

0

20S

40S

120 E

140 E

160 E

Fig. 22.1 Japanese longline fishing effort in Australian waters from 1991 to 1995 (33,575 sets).

Table 22.2 Comparison of blue shark catch, effort, and catch per unit effort (CPUE) from logbook and observer data from Japanese longline vessels fishing in Australian waters from 1992 to 1996.* Region

East East East East West West

Latitude

10–20°S 20–30°S 30–40°S 40–50°S
30°S 30°S

Logbook data

Observer data

Catch

Effort

3,205 5,816 18,554 269,893 2,844 70,875

6,073,973 8,359,356 16,988,093 36,076,252 2,949,272 7,367,206

CPUE

Catch

Effort

0.53 0.70 1.09 7.48 0.96 9.62

443 1,000 2,224 30,295 44 3,506

333,870 792,942 1,130,660 3,935,932 79,261 517,786

CPUE 1.33 1.26 1.97 7.70 0.56 6.77

*Data are separated by 10º latitude bands on the east coast, and north and south of 30º on the west coast. Catch is number of sharks, effort is number of hooks, and CPUE is number of sharks per 1,000 hooks.

Bycatch of Pelagic Sharks in Australia’s Tuna Longline Fisheries

263

The average catch rate from all regions was 4.77 from logbook data and 5.52 from observer data. Using the total Japanese effort of 77,814,152 hooks (Table 22.2), together with the observer catch rate, suggests a total catch of 429,534 blue sharks over 5 years. We converted these numbers to weight using the length–frequency distributions of the catch stratified by latitude (Fig. 22.2 shows that size decreases to the south) and a locally derived length–weight relationship. Our resulting estimated annual catch over the 1992–1996 period was 1,800 metric tons (t). This estimate, using the observer catch rate, is about 14% higher than if the logbook catch rates are used. An annual catch of 1,100 t was reported in Stevens and Wayte (1999) using the same catch rate and effort figures; however, numbers were converted to weights using a less robust method. Using observer data, West et al. (2004) estimated that about 230 t (with a 95% confidence range of 128–331 t) of blue sharks were caught by domestic vessels in the year 2000. The declared logbook catch from domestic vessels for the same period was 307 t. In the region 20–40°S, where the majority of the Australian longline effort occurs, there was a four- to five-fold decrease in catch rates between those observed on Japanese vessels during the period 1991–1997 and those observed on domestic vessels mainly during the period 2001–2003 (West et al., 2004). There are a number of possible explanations for this. There may have been a real decrease in blue shark abundance in the region between the two data collection periods, which could be due to localized depletion by the domestic fleet, oceanwide reductions in blue shark numbers, or a change in blue shark spatial distribution. The differences could also be attributed to variations in fishing practice between the domestic and Japanese fleets. This could arise from different gear construction, setting and soak times, or fishing areas. There is some suggestion that blue shark abundance is lower inshore (
100 km from the coast) from where most of the domestic observer data were collected. A routine domestic observer program commenced in mid-2003 and will greatly improve the amount of observer-collected data for the domestic longline fleet. It will be important to use these data to improve the estimates of the domestic catch of blue shark in the fishery and to verify (or update) the preliminary estimates given here. The catch rate for shortfin makos (all areas combined) was 0.18 from logbook data and 0.20 from observer data for the Japanese fishery. Agreement between logbook and observer data was generally good. Using the total Japanese effort of 77,814,152 hooks, together with the observer catch rate, suggests a total catch of 15,563 shortfin makos over the 5-year period (167 t/year). The highest observer catch rates in the Japanese fishery occurred in the 20–30°S (0.50) and 30–40°S (0.40) regions on the east coast, and in the 30°S (0.30) region on the west coast, but there was no clear latitudinal trend in the data. In the more limited domestic data (1996–1997), the highest catch rates were in the 30–40°S (0.38) and 40–50°S (0.26) regions of the east coast. The majority of porbeagle sharks were caught offshore from Tasmania, and so the comparison of Japanese logbook and observer catch data was restricted to the east coast area south of 39°S. The average catch rate in this area from logbook data was 0.25, compared to 0.54 from observer data, over the period 1991–1996. This suggests that a total catch of 24,213 porbeagles was taken around Tasmania by an effort of 44,839,313 hooks over the 5-year period (139 t/year). Agreement between logbook and observer data was reasonably poor, particularly for the latter years, with catch rates from both sources generally increasing with time. This may reflect better recording and, in the case of observers, better identification

264

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Males 30

Females 30

10–20S n  85

20

20

10

10

0

10–20 S n  62

0 0

30

50

100

150

200

250

300

0

30

20–30S

100

150

200

250

300

100

150

200

250

300

100

150

200

250

300

150

200

250

300

20–30S

n  565

Percent frequency

50

n  286

20

20

10

10

0

0 0

30

50

100

150

200

250

300

0

30

30–40S

50

30–40 S n  481

n  665 20

20

10

10

0

0 0

30

50

100

150

200

250

300

0

30

40–50S

50

40–50 S

n  4,207

n  9,415

20

20

10

10

0

0 0

50

100

150

200

250

300

0

50

100

Fork length (cm) Fig. 22.2 Fork length (cm) composition by area and sex of blue sharks taken by Japanese longline vessels off the east coast of Australia from 1991 to 1996 (based on observer data).

Bycatch of Pelagic Sharks in Australia’s Tuna Longline Fisheries

265

of this shark, which in the earlier years was often confused with the shortfin mako. The catch rate of porbeagles from domestic vessels in 1997 from 40°S to 50°S on the east coast (the only area and year for which sufficient data were available) was 0.70.

Length and sex composition The length composition of blue sharks taken by Japanese longliners is shown by latitude and sex for the east coast in Fig. 22.2. Length decreased toward the south. In the 10–20°S and 20–30°S areas, the length frequency consisted of relatively large fish, with a single mode for both sexes between 200 and 230 cm fork length. At 30–40°S, these larger fish were present, but there was an additional group of smaller fish of both sexes with a modal length of about 100 cm. At 40–50°S, only these smaller fish were present and there were very few individuals of more than 200 cm; for females, however, there was another mode at 160–170 cm. The sex ratio was about 1:1 in the most northern region, there were more males between 20°S and 40°S, and there was a much higher proportion of females at 40–50°S (Table 22.3). No clear latitudinal trend was apparent for shortfin mako size or sex ratio on the east coast (Tables 22.4 and 22.5), although more females were caught at 20–30°S. The porbeagle catch comprised mainly 1-year olds with a modal length of about 100 cm and a sex ratio of about 1:1.

Table 22.3 Sex composition by area of blue shark catches from Japanese longline vessels fishing in Australian waters from 1991 to 1996, based on observer data. Region

Latitude

Males

Females

East East East East West West

10–20°S 20–30°S 30–40°S 40–50°S
30°S 30°S

170 664 873 7,460 35 822

165 330 710 19,262 55 428

pa

% female 49 33 45 72 61 34

ns ** ** ** * **

χ test on variance from 1:1 sex ratio. ns: not significant. *p
0.05; **p
0.01.

a 2

Table 22.4 Fork length (cm) composition by area and sex of shortfin makos taken by Japanese longline vessels fishing in Australian waters from 1992 to 1996.* Region

East East East West

Latitude

20–30°S 30–40°S 40–50°S 30°S

Minimum

Maximum

Mode

M

F

M

F

M

F

M

F

82 67 67 68

77 65 73 61

252 265 350 256

295 327 305 296

98 193 126 107

162 104 130 174

195 234 185 52

251 178 160 65

*M: males; F: females. There were insufficient data for areas 10–20°E and
30°W.

n

266

Sharks of the Open Ocean

Table 22.5 Sex composition by area of shortfin mako catches from Japanese longline vessels fishing in Australian waters from 1991 to 1996, based on observer data. Region

Latitude

Males

Females

East East East East West West

10–20°S 20–30°S 30–40°S 40–50°S
30°S 30°S

19 220 259 225 7 56

23 288 206 186 1 72

pa

% female 55 57 44 45 13 56

ns ** * ns * ns

χ test on variance from 1:1 sex ratio. ns: not significant. *p
0.05; **p
0.01.

a 2

30

Logbook data

1992

20

20

10

10

0 Catch rate (number per 1,000 hooks)

30

1993

Observed data

0 0

30

2

4

6

8

10

12

0

30

1994

20

20

10

10

0 0

30

2

4

6

8

10

4

8 6 Week

10

12

0

2

4

6

8

10

12

1995

0

2

4

6

8

10

12

1996

20 10 0 0

2

12

Fig. 22.3 Japanese longline catch rates for blue sharks at 40–50°S on the east coast of Australia between May 1 and July 30, from 1992 to 1996.

Bycatch of Pelagic Sharks in Australia’s Tuna Longline Fisheries

267

Stock status Of particular interest is the question of how resilient stocks of pelagic sharks are to the impacts of fishing. Any assessment of the impact of Japanese longlining on pelagic shark stocks in Australian waters is limited by the current restricted time-series of catch and effort data. In addition, species-specific catch data were really only sufficient for blue sharks. Given the relatively high fishing effort exerted by the Japanese between 40°S and 50°S on the east coast between May and July, we were interested to see how the catch rates of blue sharks changed in this area during the fishing season. If fishing was having an impact on the stock, it might be expected that the catch rate would decline as the season progressed. This assumes that there is minimal immigration or emigration of blue sharks over this period. However, no consistent trend was apparent, with catch rates showing a general increase with time in 1992 and 1993, an initial decline followed by a subsequent increase in 1994 and 1995, and a general decline (at least in the observed catch rate) in 1996 (Fig. 22.3).

Acknowledgments We would like to thank Tim Jones, Ann Preece, André Punt, and Grant West (CSIRO Marine and Atmospheric Research), Hein Sturmann (Australian Fisheries Management Authority), and Terry Walker (Primary Industries Research Victoria) for help with various aspects of this project. We are grateful to Malcolm Francis (National Institute of Water and Atmospheric Research, Wellington) for helpful comments on the manuscript. This work was funded by Fisheries Research and Development Corporation grant 98/107.

References Stevens, J. D. (1992) Blue and mako shark by-catch in the Japanese longline fishery off southeastern Australia. In: Sharks: Biology and Fisheries (ed. J. G. Pepperell). Australian Journal of Marine and Freshwater Research 43(special volume), 227–236. Stevens, J. D. and Wayte, S. E. (1999) A Review of Australia’s Pelagic Shark Resources. Fisheries Research and Development Corporation Project 98/107. CSIRO Marine Research, Hobart, Tasmania, Australia, 64 pp. Ward, P. J. (ed.) (1996) Japanese Longlining in Eastern Australian Waters 1962–1990. Bureau of Resource Sciences, Canberra, Australian Capital Territory, Australia, 249 pp. West, G., Stevens, J. and Basson, M. (2004) Assessment of Blue Shark Population Status in the Western South Pacific. Australian Fisheries Management Authority Project R01/1157. CSIRO Marine Research, Hobart, Tasmania, Australia, 139 pp.

Chapter 23

Case Study: Catch and Management of Pelagic Sharks in Hawaii and the US Western Pacific Region Paul J. Dalzell, R. Michael Laurs and Wayne R. Haight

Abstract The shark catch component of pelagic fisheries in Hawaii and the US western Pacific region (WPR) is summarized for longline, troll, handline, and purse-seine gears. There is little market demand for shark flesh in the WPR, and most sharks were retained for their fins only until State of Hawaii and federal bans in 2000 ended this practice. Shark catches in the Hawaii longline fishery have declined from a peak in the early 1990s, because of increased targeting of deep-swimming tunas and a ban on shallow-set longline fishing for swordfish. Catch rates of blue and thresher sharks in this fishery have also declined, while mako shark catch per unit effort (CPUE) has been more variable, increasing up to 1998 and then declining. Pelagic shark catches in Hawaii troll and handline fisheries peaked in the early 1990s and declined thereafter. This drop in catches was also matched by a decrease in CPUE in both troll and handline fisheries. Recently implemented and planned shark management measures in the WPR include revision of the Pelagic Management Unit to include only nine species of pelagic sharks, and a possible trip limit for all longline-caught pelagic sharks other than blue sharks in the Hawaii longline fishery. Key words: Hawaii, Pacific Ocean, western Pacific region, CPUE, blue shark, management, shark finning, fin trade.

Introduction This case study presents a synopsis of catches and catch rates of fisheries that are capturing pelagic sharks in the US western Pacific region (WPR), and reviews the economic and management issues associated with pelagic shark catches. The WPR comprises the exclusive economic zones around Hawaii, American Samoa, the Northern Mariana Islands (NMI), and a number of small islands and atolls in the central Pacific. Pelagic fishing methods in the WPR include longlining (Hawaii and American Samoa), trolling (Hawaii, Guam, American Samoa, NMI), pelagic handlining (Hawaii), pole-and-line fishing (Hawaii), and Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

Pelagic Sharks in Hawaii and the Western Pacific Region

269

purse-seining (central and western Pacific). Pelagic sharks commonly taken by US fisheries in the WPR include the blue (Prionace glauca), silky (Carcharhinus falciformis), and oceanic whitetip (C. longimanus) sharks of the Carcharhinidae, bigeye thresher (Alopias superciliosus, Alopiidae), and shortfin mako (Isurus oxyrinchus, Lamnidae). Other pelagic sharks caught by pelagic fisheries, albeit rarely, include the common thresher (A. vulpinus), longfin mako (I. paucus), pelagic thresher (A. pelagicus), and salmon shark (Lamna ditropis, Lamnidae). Mako and thresher shark landings are reported in aggregate in the WPR and not by individual species. Other sharks also caught occasionally by pelagic fisheries in the WPR include hammerheads (Sphyrnidae) and the carcharhinid Galapagos (C. galapagensis) and tiger (Galeocerdo cuvier) sharks. Stevens (2000) gave a general overview of the biology and fisheries of pelagic sharks taken in Pacific fisheries, while Smith et al. (1998, 2008) evaluated Pacific pelagic elasmobranchs for their resilience to fishing. Nakano (1994) and Nakano and Seki (2002) presented an in-depth review of the biology of blue sharks in the North Pacific, and the US National Marine Fisheries Service conducted a stock assessment of blue sharks in the North Pacific (Kleiber et al., 2001).

Catches and catch rates Sharks are not targeted by the US pelagic fisheries of the WPR, and detailed information on shark catches and catch rates are not published, other than for the Hawaii longline fishery. The average annual catches of sharks in these fisheries were thus obtained firsthand from various fishery agencies (Table 23.1). The Hawaii longline fishery catches the Table 23.1 Average annual catch of sharks in pelagic fisheries of the WPR. Location

Fishery

Annual average catch (t)

Period

Principal shark species

Source

Hawaii

Pelagic longline

4,168

1991–2005

Blue, makos, threshers

Hawaii

1.3

1986–2005

Hawaii

Pelagic handline Troll

2.8

1986–2005

Guam

Troll

2.5

1996–2004

Makos, threshers, hammerheads, tiger Makos, threshers, hammerheads, tiger Silky, Galapagos, oceanic whitetip

American Samoa

Troll

0.2

1996–2004

Blue, makos, threshers

American Samoa

Pelagic longline

280

1996–2005

Blue, makos, threshers

Centralwestern Pacific

Tuna purse seine

105

1998–2004

Silky, oceanic whitetip, blue

Ito and Machado (2001); R. Ito (personal communication) Hawaii Division of Aquatic Resources, Honolulu Hawaii Division of Aquatic Resources, Honolulu NMFS Pacific Islands Fisheries Science Center, Honolulu NMFS Pacific Islands Fisheries Science Center, Honolulu Western Pacific Fisheries Information Network, Honolulu Anonymous (2006); P. Williams (personal communication)

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Sharks of the Open Ocean

largest volume of sharks, with an annual average of more than 4,100 metric tons (t) for the period 1991–2005, followed by the American Samoa longline fishery and the US purseseine fishery operating in the western and central Pacific. The relatively modest American Samoa longline fishery began in the mid-1990s; through 1999 it had landed less than 500 t of tuna annually, then the fishery expanded markedly until 2002, when its tuna catches were equivalent to those of the Hawaii fishery (⬎5,000 t; WPRFMC, 2003). Nevertheless, the 2004 shark catch amounted to only 680 t, or about 16% of the long-term average for the Hawaii fishery. At present, more than 90% of the US longline and purse-seine shark catch is not retained. Previously, up to two-thirds of the Hawaii longline shark catch was retained for finning, but this declined to about 5% after 2000, following federal and state bans on shark finning (see below). Catches of pelagic sharks in the Hawaii longline fishery rose to a peak in 1993, declined until 2001, and then began to show a modest increasing trend thereafter (Fig. 23.1). Most of the decline between 1993 and 2001 is thought to be from operational and management changes in the Hawaii fishery, because there was a shift after 1993 from shallow-set longlining for swordfish to deeper sets for bigeye tuna. Pelagic sharks make up about 50% of the catch composition of shallow swordfish longline sets, compared to 16% for tuna sets (Ito and Machado, 2001; R. Y. Ito, personal communication). The increasing catch following 2001 may be due to increases in fishing effort for tuna to the north of the Hawaiian Islands, where blue sharks are more abundant (R. Y. Ito, personal communication). The catch of pelagic sharks in the Hawaii troll and handline fisheries peaked in 1990–1992, then followed a generally declining trend through 2005 (Fig. 23.2). Normalized catch per unit effort (CPUE) data for the Hawaii longline fishery and the troll and tuna handline fisheries are also shown in Figs. 23.1 and 23.2. CPUE is reported separately for blue sharks, threshers, and mako sharks in the longline fishery, which can

Catch Blue shark CPUE Mako CPUE Thresher CPUE

7,000

Catch (t)

6,000

4.00 3.50 3.00

5,000

2.50

4,000

2.00

3,000

1.50

2,000

1.00

1,000

0.50

0

Normalized CPUE

8,000

0.00 1991

1993

1995

1997

1999

2001

2003

2005

Year Fig. 23.1 Catch and CPUE of pelagic sharks caught in the Hawaii longline fishery, 1991–2005.

Pelagic Sharks in Hawaii and the Western Pacific Region

9.00

Catch Troll CPUE Handline CPUE

8.00 7.00

4.00 3.50

2.50

5.00 2.00 4.00 1.50

3.00

Normalized CPUE

3.00

6.00 Catch (t)

271

1.00

2.00

0.50

1.00 0.00

0.00 1986

1990

1994

1998

2002

Year Fig. 23.2 Catch and CPUE of pelagic sharks caught in the Hawaii troll and tuna handline fisheries, 1986–2005.

be verified through observer data. Most of the Hawaii longline shark catch (90–98%) is blue shark, with smaller amounts of makos and threshers (Ito and Machado, 2001). Catch data for pelagic sharks taken by the troll and handline fisheries are most often reported as aggregate total catch, and are rarely broken down by species. Those species reported in the data are makos, threshers, hammerheads, and tiger sharks.

Stock status Little information exists on the stock status of most pelagic sharks in the WPR. Nakano and Watanabe (1992) estimated that the North Pacific blue shark standing stock ranged from 52 to 67 million sharks, based on drift-net data from the late 1980s. More recently, Kleiber et al. (2001) conducted a detailed stock assessment of the North Pacific blue shark using the MULTIFAN-CL length-based, age-structured model (Fournier et al., 1998), and included data on catch and size frequencies from the Hawaii and Japanese longline fisheries, as well as the now defunct Japanese high-seas drift-net fishery. The impetus for this stock assessment was the large numbers of blue sharks that, until recently, were retained and finned by the Hawaii longline fishery, with the carcasses discarded. Kleiber et al. (2001) concluded that even the most conservative scenarios suggest that the maximum sustainable yield lies between two and four times current catches (⬃140,000 t; Stevens, 2000). Clarke (2003) reached a similar conclusion using a surplus production model, with biomasses extrapolated from shark fin data. However, West et al. (2004) cautioned that blue shark productivity in the South Pacific was limited to between 4% and 12% of the unfished biomass, depending on the age at which the sharks become vulnerable to fishing. Oshiya (2000), using an age-structured dynamic production model to assess silky sharks in the tropical and subtropical Pacific, concluded that current levels of silky

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catches by purse-seiners and longliners are sustainable. It should be noted, however, that in the years following this assessment, longline and purse-seine fleets and effort levels have increased markedly in the Pacific (Kinan and Dalzell, 2005; Lawson, 2005). Stock assessments for other pelagic sharks in the Pacific have not been conducted.

Economics and management Small amounts of shark meat are landed in the WPR, where in general it is not held in much esteem. Even species with relatively high-quality flesh, such as makos and threshers, are in little demand in the region. Until 2000, the main shark product traded in the WPR was shark fin. McCoy and Ishihara (1999) investigated the shark fin trade in the WPR using a variety of data sources, including logbooks, transshipment records, and customs records, to estimate the volume of shark fins landed from domestic and foreign fishing vessels in American Samoa, Guam, and Hawaii. Information on fin value was obtained from interviews with shark fin dealers in these locations. Most of the fin trade traditionally was associated with foreign fishing vessels that either landed fins directly into ports not covered by the Nicholson Act (Guam, American Samoa) or transshipped their fins at sea to US vessels that then landed in Hawaii for onward transshipment (McCoy and Ishihara, 1999). The rise in the value of blue shark fins in the mid-1990s led to an increase in finning activity on Hawaii-based longline vessels, where 65–70% of the blue sharks captured were finned. The domestic fin trade from these vessels was thought to be worth $1 million, with an additional transshipment of foreign fins worth a minimum of $2.5 million. Foreign transshipment of fins through Guam and American Samoa was estimated to be worth about $0.7 million (McCoy and Ishihara, 1999). In August 2000, the State of Hawaii banned the landing of shark fins without the accompanying carcass. This was followed by a US federal shark finning ban implemented in February 2002. The Hawaii ban effectively ended the practice of shark finning in the Hawaii longline fishery, and the federal ban has terminated the legal transshipment through Guam and American Samoa of fins caught by foreign vessels. Pelagic fisheries in the federal waters of the WPR are managed through the Western Pacific Council’s Pelagic Fisheries Management Plan (PFMP), which was published in 1986. The PFMP originally defined the sharks belonging to the management unit as “oceanic sharks of the families Alopiidae, Carcharhinidae, Lamnidae and Sphyrnidae.” This definition meant that a considerable number of primarily coastal sharks, such as tiger shark, sandbar shark (Carcharhinus plumbeus), Galapagos shark, and hammerheads, were also included under the PFMP. In 2002, however, the Council published a Coral Reef Fishery Ecosystem Fishery Management Plan (CREFMP) that also amended the PFMP management unit to include only nine pelagic sharks, while coastal sharks would be managed under the CREFMP. The pelagic management unit now contains only silky shark, oceanic whitetip shark, blue shark, salmon shark, shortfin and longfin makos, and pelagic, bigeye, and common threshers. The Council is currently conducting research on whether it should place a precautionary limit on how many threshers, makos, and other pelagic sharks may be landed on each trip, in the absence of stock assessments for these species.

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Conclusions The targeting and retention of sharks by US vessels in the western Pacific are not likely to increase above current levels, particularly following the ban on shark finning, which represented the principal economic market for sharks in the region. Sharks are not highly valued in the islands of the US western Pacific, and it is not economically viable to fish for pelagic sharks for export markets. Longline fisheries in the region take the largest volume of pelagic sharks, but both the Hawaii and American Samoa longline fisheries have limited-entry programs that cap fleet size. The US purse-seine fleet shrunk from 62 vessels in 1983 to 21 vessels in 2004 (Lawson, 2005), while small-scale troll and handline fleets have remained steady or declined in the western Pacific and take only small amounts of pelagic sharks (WPRFMC, 2003). However, fishing mortality on pelagic sharks may increase as the much larger longline and purse-seine fleets of other Pacific nations continue to expand (Lawson, 2005). In the absence of stock assessments for pelagic sharks, trends in pelagic shark CPUE in Hawaii should continue to be monitored to determine if they simply reflect changes in local abundance or may be indicative of the status of pelagic sharks in the North Pacific.

Acknowledgments We thank colleagues in the NMFS Honolulu Laboratory, NMFS Pacific Islands Area Office, Hawaii Division of Aquatic Resources, and the Oceanic Fisheries Program of the Secretariat of the Pacific Community for their assistance.

References Anonymous (2006) A description of observer and port sampling data collected under the US Multilateral Treaty and FSM Arrangement. Internal Meeting of Pacific Island Parties to the South Pacific Regional US Multilateral Treaty, 6–8 March 2006, Honolulu, Hawaii. Oceanic Fisheries Program, Secretariat of the Pacific Community, Noumea, New Caledonia. Clarke, S. C. (2003) Quantification of the Trade in Shark Fins. Ph.D. thesis, Imperial College London, London, UK. Fournier, D. A., Hampton, J. and Sibert, J. R. (1998) MULTIFAN-CL: A length-based, age-structured model for fisheries stock assessment, with application to South Pacific albacore, Thunnus alalunga. Canadian Journal of Fisheries and Aquatic Sciences 55(9), 2105–2116. Ito, R. Y. and Machado, W. A. (2001) Annual Report of the Hawaii-Based Longline Fishery for 2000. Administrative Report H-01-07. Southwest Fisheries Science Center, NOAA/NMFS, Honolulu, HI. Kinan, I. and Dalzell, P. (2005) Sea turtles as flagship species. Maritime Studies (MAST) 3(2), 195–212. Kleiber, P., Takeuchi, Y. and Nakano, H. (2001) Calculation of Plausible Maximum Sustainable Yield (MSY) for Blue Sharks (Prionace glauca) in the North Pacific. Administrative Report H-01-02. Southwest Fisheries Science Center, NOAA/NMFS, Honolulu, HI. Lawson, T. (2005) Western and Central Pacific Fisheries Commission Tuna Fishery Yearbook 2004. Oceanic Fisheries Program, Secretariat of the Pacific Community, Noumea, New Caledonia.

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McCoy, M. and Ishihara, H. (1999) The Socioeconomic Importance of Sharks in the US Flag Areas of the Western and Central Pacific. Administrative Report AR-SWR-99-01. Southwest Fisheries Science Center, NOAA/NMFS, Honolulu, HI. Nakano, H. (1994) Age, reproduction and migration of blue shark in the North Pacific Ocean. Bulletin of the National Research Institute of Far Seas Fisheries 31, 141–256. Nakano, H. and Seki, M. P. (2002) Synopsis of biological data on the blue shark, Prionace glauca Linnaeus. Bulletin of the Fisheries Research Agency 6, 18–55. Nakano, H. and Watanabe, Y. (1992) Effect of high seas driftnet fisheries on blue shark stock in the North Pacific. In: Compendium of Documents Submitted to the Scientific Review of North Pacific High Seas Driftnet Fisheries. Sidney, British Columbia, Canada, 11–14 June 1991. Oshiya, S. (2000) Biological Study and Stock Assessment of Silky Shark (“Kurotogarizme”) Carcharhinus falciformis in the Tropical and Subtropical Pacific Ocean. M.Sc. thesis, School of Marine Science and Technology, Tokai University, Shimizu, Japan. Smith, S. E., Au, D. W. and Show, C. (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678. Smith, S. E., Au, D. W. and Show, C. (2008) Intrinsic rates of increase in pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Stevens, J. (2000) The population of highly migratory oceanic sharks. In: Getting Ahead of the Curve: Conserving the Pacific Ocean’s Tunas, Swordfish, Billfishes and Sharks (ed. K. Hinman). National Coalition for Marine Conservation, Leesburg, VA. West, G., Stevens, J. and Bassoon, M. (2004) Assessment of Blue Shark Population Status in the Western South Pacific. Prepared for CSIRO Marine Research and the Australian Fishery Management Authority, AFMA Project R01/1157. AFMA, Barton, Australian Capital Territory, Australia, 139 pp. Western Pacific Regional Fishery Management Council (WPRFMC) (2003) Pelagic Fisheries of the Western Pacific Region: 2002 Annual Report. WPRFMC, Honolulu, HI.

Chapter 24

Case Study: Pelagic Shark Fisheries along the West Coast of Mexico Oscar Sosa-Nishizaki, J. Fernando Márquez-Farías and Carlos J. Villavicencio-Garayzar

Abstract Mexican fisheries landed an annual average of 28,952 metric tons of sharks from 1992 to 2002, of which 67% was caught off the Pacific Coast. The most important pelagic species landed were the blue shark, threshers, hammerheads, and the silky shark. The major fisheries targeting sharks along the west coast of Mexico are the artisanal fishery, the pelagic longline fishery, and the gill-net fishery. Regulations have recently enforced and prohibit shark finning, established protected areas, required the use of logbooks, and set standards for the type and design of fishing gears. Key words: artisanal fishery, longline fishery, gill-net fishery, Gulf of California, Mexico, Mexican Pacific, regulations.

Introduction Mexico is one of the most important elasmobranch-fishing nations in the world. Shark fishing represented 2.1% by weight of the national fishery production from 1992 to 2002, with annual average landings of 28,952 metric tons (t) (SAGARPA, 2004a). The Pacific Coast of Mexico contributed 67% of the total shark landings during this period. No data on catches by species are available (Castillo-Géniz, 1992; Bonfil, 1994). Shark fisheries currently represent an important source of food and employment on both coasts of Mexico (Castillo-Géniz et al., 1998). Sharks and rays are traditionally used for food, either fresh, frozen, or, more commonly, salt-dried. Shark fins and hides are also exported and the offal is reduced to fishmeal (Bonfil, 1994). Recently shark skin has been used in the leather business and cartilage in the natural medicine trade. Shark landings from the Pacific Coast began increasing in the late 1970s, reaching a high of 25,534 t in 1981 (Table 24.1). Landings declined for the rest of the 1980s, then rose to 23,248 t in 1993; they averaged 18,913 t from 2000 to 2002. In the 1980s to mid-1990s, many of the pelagic shark species were finned and discarded at sea, but this Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Table 24.1 Reported shark landings for the Mexican Pacific Coast (Castillo-Géniz, 1992; SAGARPA, 2004b). Year

Landings (t)

Year

Landings (t)

1976 1977 1978 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989

14,214 14,777 16,691 20,325 20,939 25,534 24,114 17,493 18,364 15,778 16,843 15,103 19,794 17,581

1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002

22,936 20,714 20,567 23,248 23,197 21,022 20,965 15,441 15,940 15,315 19,965 18,512 18,261

practice is declining in some regions because of the development of new markets, especially for blue shark meat. The major fisheries targeting pelagic sharks within the exclusive economic zone (EEZ) off Mexico’s Pacific Coast are the artisanal fishery, the pelagic longline fishery, and the gillnet fishery. Together, they operate along the entire coast, including the Gulf of California, and target a wide variety of sharks as well as valuable teleosts (Holts et al., 1998). The principal species of pelagic sharks exploited by these fisheries are three species of the family Alopiidae, the common thresher (Alopias vulpinus), bigeye thresher (A. superciliosus), and pelagic thresher (A. pelagicus); the shortfin mako (Isurus oxyrinchus, Lamnidae); and the blue shark (Prionace glauca) and blacktip shark (Carcharhinus limbatus) of the Carcharhinidae family, as well as silky shark (C. falciformis, sometimes misidentified as blacktip shark) and oceanic whitetip shark (C. longimanus) (Galván-Magaña et al., 1989; Holts et al., 1998; Márquez-Farías, 2002; Mendizábal y Oriza et al., 2002; SorianoVelásquez et al., 2002). Several other species, some of which occupy coastal-pelagic habitats, are also taken, such as hammerhead sharks (Sphyrna spp., Sphyrnidae) and the carcharhinid species bull shark (C. leucas), dusky shark (C. obscurus), tiger shark (Galeocerdo cuvier), and Pacific sharpnose shark (Rhizoprionodon longurio).

Artisanal fishery Subsistence shark fisheries along the Pacific Coast of Mexico have long been an important resource to rural communities. The multispecies artisanal shark fishery operates on the seasonal abundance of a number of shark and teleost species (Castillo-Géniz et al., 1998). Fishing is done from pangas, which are small (7–10 m long), outboard-powered open boats. They can range as far as 100 km from shore, but usually they fish closer. Trips are limited to 1 or 2 days because there are no cooking, sleeping, or storage facilities onboard (Holts et al., 1998). Depending on the region and time of year, fishing gears can include small bottom longlines (referred to as cimbras or palangres), pelagic longlines (around 500 hooks),

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small drift gill nets, and bottom fixed gill nets. The gear is set and hauled by hand (Bonfil, 1994), and tends to catch a variety of species. The catch is stored in the bottom of the panga without ice. There have been no official records of the type and number of vessels involved in this fishery, or the number of trips taken, but a recent survey determined that 4,937 pangas participated in this fishery along the entire Mexican Pacific Coast (SAGARPA, 2004a). The artisanal shark fishery off Puerto Morelos, Chiapas (the most southern shark fishery in Mexico), targets mainly coastal sharks, but also takes a substantial percentage of pelagic sharks (Soriano-Velásquez et al., 2002). However, because of the seasonal latitudinal migration of the shark populations, fishermen from Chiapas move north along the Mexican coast to establish temporary fishing camps, mainly in Nayarit, Sonora, and the east coast of Baja California in the Gulf of California, there competing with the local fishermen. The species caught in this region are mostly thresher, silky, and hammerhead sharks. Sometimes these species use areas of the Gulf of California for reproduction, so fishing grounds can overlap with nursery areas (Márquez-Farías, 2002). Landing places have very limited infrastructure, and fishers process the catch on the beach. This fishery is highly weather dependent and, in some places, like Sonora and Baja California, sharks serve as an alternative target between fishing seasons for more valuable resources, such as blue crab and shrimp. Nevertheless, in some areas like the northwestern coast of Baja California, fishing for blue shark occurs year-round; this fishery has been expanding in recent years.

Pelagic longline fishery A longline fleet of large vessels (22–53 m long, both domestic and joint venture vessels) began operating in the EEZ of Mexico around 1980. Macías-Zamora et al. (1994) divided the fleet into two groups: those targeting exclusively billfishes, fishing in the central and northern Mexican Pacific in mostly large vessels, and those targeting both sailfish (Istiophorus platypterus, Istiophoridae) and sharks, along the central and southern Mexican coast. The operations of the fleet targeting billfishes were terminated in 1990 in Mexican waters. Only one large-sized longline vessel fishes under a scientific research permit to target sharks and to document species distributions and life-history information (Mendizábal y Oriza et al., 2002). This vessel catches mainly thresher, silky, and hammerhead sharks. Silky sharks are common off southern Mexico (Gulf of Tehuantepec), whereas the west coast of the Baja California peninsula produces high catches of blue shark (Mendizábal y Oriza et al., 2002). Close to the coast, 38 medium-sized vessels (10–24 m long) operate with longlines and target sharks and teleosts (Mendizábal y Oriza et al., 2002). However, data from these vessels have not been published and there has been no analysis of their operations.

Gill-net fisheries The gill-net fishery for sharks and teleosts is an important fishery, and occurs mostly near the coast. Inside the Gulf of California, this fishery is conducted by medium-sized vessels (10–17 m long) that can stay on the water for 4–15 days. Most of them use middle-water gill

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nets, but some use bottom set nets (Márquez-Farías, 2002). In 1996, 20 gill-net fishing boats were operating along the Mexican Pacific, including the Gulf of California (Mendizábal y Oriza et al., 2002). The drift gill-net fishery targets swordfish and sharks and operates mainly off the west coast of the Baja California peninsula. The gear characteristics are similar to those used in California, USA (Holts et al., 1998). Preliminary analysis has shown that sharks are the most important component of the catch (25%), with blue sharks, hammerheads, makos, and threshers being the dominant species (in order of importance); swordfish represent only 12% of the catch. Since the middle of the 1990s, some of the boats from this fishery have changed to longline operations and their main targets are now swordfish and blue shark. Most of the drift gill-net fleet (34 fishing vessels) is based at Ensenada, Baja California, and the rest (14 vessels) fish along the central Mexican Pacific and in the Gulf of California (SAGARPA, 2004b).

Shrimp trawl bycatch The bycatch from shrimp trawlers represents an important source of fishing mortality for elasmobranch populations, but mainly affects coastal species. Significant numbers of hammerhead neonates are killed every year, especially in the Gulf of California, where around 500 shrimp trawlers are based. The use of fish exclusion devices to reduce bycatch has been enforced recently. However, no regulations on the elasmobranch bycatch are currently applied to this fishery.

Fisheries interactions and stock assessment Some artisanal fisheries interact with the drift gill-net and longline fisheries by competing for the same species in adjacent or nearby areas. For example, in the blue shark fishery off the western coast of Baja California, artisanal vessels fish up to 100 km off the coast from the principal ports or fishing camps along the peninsula, whereas the medium-sized drift gill-net and longline vessels fish farther off. Furlong-Estrada (2000) found that the mean size of the blue sharks landed in Ensenada by the artisanal fishery was 119 cm in total length (TL), while the mean size for middle-sized vessels was 177 cm TL (Fig. 24.1). This shows that the combined effort from both fisheries extends the range of the size (age) of blue sharks under fishing pressure. In this situation, changes in the fishing intensity or patterns of one fishery may affect the catches of the other fishery; however, no further studies have analyzed these potential effects in either the catches or the stock levels of the blue shark. No formal assessment has been conducted for pelagic sharks in the Mexican Pacific. However, analyses of the catch trends by region have indicated the depletion of some of the shark and ray populations. Márquez-Farías (2002) reported that shark production from the states of Sonora and Sinaloa decreased by about 60% from 1976 to 1999, and that most of the catch was taken in the Gulf of California. Using catch and effort trends from the shark longline fishery based at Manzanillo, Colima, from 1986 to 1999, Mendizábal y Oriza et al. (2002) suggested that most of

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279

300 Drift gill-net and longline

Number of sharks

250

Artisanal fishery

200 n
2,186 150

100

50

65 75 85 95 105 115 125 135 145 155 165 175 185 195 205 215 225 235 245 255 265 275 285

0

Total length (cm) Fig. 24.1 Blue shark (Prionace glauca) size frequency distribution (n
2,186) from the artisanal and mediumsized drift gill-net and longline catches landed at Ensenada, Mexico, during 1999–2000 (Furlong-Estrada, 2000).

the pelagic shark species (blue, blacktip, silky, and scalloped hammerhead sharks) have reached their maximum catch levels. They also reported that the pelagic thresher showed a decline in its catch rate during the period, dropping from a mean value of 2.97 sharks per 100 hooks during 1986–1989 to 0.65 sharks per 100 hooks during the 1997–1999 period. On the basis of this information, they recommended that the federal government impose a moratorium on pelagic shark fishing, adopt closed seasons for different periods and areas for each of the shark species, and declare the pelagic thresher shark to be overfished. Unfortunately, none of these regulations has been issued as of the time of writing.

Regulations Despite the socioeconomic importance of shark fishing in Mexico, very few regulations have been implemented for this fishery. Since the 1970s, fishermen have been required to obtain an annual shark-fishing permit and report landings of all groups of fish and shark species caught. At the beginning of the 1990s, the demand for shark-fishing permits increased, but because the status of most shark populations was unknown, the Mexican National Institute of Fisheries recommended a moratorium on issuing new shark-fishing permits beginning in 1993 (Castillo-Géniz et al., 1998). A moratorium on permits for medium- and large-sized boats was implemented in 1998 and no new permits have been issued since (J. L. Castillo-Géniz, personal communication). Also during the 1990s, the federal government developed the Mexican Official Standards (or NOMs) to manage the most important fisheries. These NOMs are legally binding management measures that are proposed by federal authorities, signed by fishermen

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organizations, and amended by the Mexican Congress. NOMs include the traditional command-and-control regulations such as permits, gear specifications, season and area closures, size limits, quota limits, and modifications of fishing gear or operations to avoid bycatch. The procedure to enact or change a NOM takes a long time because federal law requires that all the stakeholders be consulted before a NOM can be enacted (Hernandez and Kempton, 2003). In 1996, the National Consultative Committee for Sustainable Fisheries formed a technical stakeholders group to draft a NOM to regulate shark and related-species fisheries in Mexico. The process has been long and tortuous, and continues today. After several consultations and analyses of the fisheries for sharks and related species, a draft of NOM-029-PESC-2000 was published in the Official Gazette for public discussion in January 2000 (SEMARNAP, 2000). These fishing standards would establish the type and design of fishing gear to be used in the artisanal and large-scale shark fisheries off the Pacific and Gulf of Mexico coasts. They would prohibit increases in fishing effort for the artisanal and middle-sized fishing vessels, but would allow an increase in the number of vessels targeting pelagic sharks. The NOM also sought to establish a series of protected areas in the coastal zone, mostly to protect shark nursery grounds, and would ban the practice of shark finning at sea by requiring that the number of fin sets match the number of carcasses at landing. Furthermore, it sought to prohibit fishing for some species, and required the use of logbooks to record species composition information. After 2 years of consultations, the final version of NOM-029-PESC-2000 was published in July 2002. The new standards were supposed to come into force 60 days after their publication; however, billfish sportfishing and nongovernmental organizations pressured the Mexican Congress to stop implementation to allow for additional discussion. Their main concerns were that medium-sized vessels would be allowed to fish within 1 km of the coastline and that large longline vessels would be allowed to continue operating, with a potential increase in their number. They also wanted the NOM to include clear regulations about bycatch, especially for sea turtles and marine mammals. As a result of these concerns, the federal government announced the postponement of the NOM implementation in September 2002. Further shark fisheries technical group meetings failed to generate an agreement, and a month later the NOM-029-PESC-2000 was withdrawn (SAGARPA, 2002). Because of the importance of the shark fishery in Mexico, the technical groups did not dissolve and the discussion continued under the leadership of several secretaries of the Mexican federal government. A new version of the NOM—NOM-029-PESC-2006—was published in February 2007 and enforcement began in May. These regulations prohibit shark finning and drift gill-net fishing by medium-sized vessels, and establish fishing areas by fishery, as well as nonfishing (protected) areas. They also standardize the allowed fishing gear and enforce the use of logbooks in all fisheries. Furthermore, the NOM prohibits the fishing of several species of sharks and rays.

Conclusions Shark fishing has been important for Mexican fishermen since the end of the 1800s, when export of shark fins to the Chinese market began (Castillo-Géniz, 1992). Today, pelagic

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shark meat, including that from blue sharks, is an important and cheap food source that is consumed fresh or dried and salted, while fins represent an important source of income. Recently several research centers and state universities have started elasmobranch research programs with the goal of producing the basic biological and fishery information that is needed to improve our knowledge of these species and to support the necessary management measures. Many stakeholders recognize the need for better fishery management for pelagic sharks in Mexico. Yet the commercial fishing industry is against the banning of the drift gill-net fishery, and billfish sportfishing organizations remain opposed to longline fishing in Pacific waters (Sosa-Nishizaki, 1998). With this continued lack of agreement among interest groups, the future of NOM-029-PESC-2006 and shark fishery management in Mexico remains uncertain.

References Bonfil, R. (1994) Overview of World Elasmobranch Fisheries. FAO Fisheries Technical Paper No. 342. FAO, Rome, Italy, 119 pp. Castillo-Géniz, J. L. (1992) Diagnóstico de la pesquería de tiburón en México. Instituto Nacional de la Pesca, Mexico City, Mexico, 62 pp. Castillo-Géniz, J. L., Márquez-Farías, J. F., Rodriguez de la Cruz, M. C., Cortés, E. and Cid del Prado, A. (1998) The Mexican artisanal shark fishery in the Gulf of Mexico: Towards a regulated fishery. Marine and Freshwater Research 49, 611–620. Furlong-Estrada, E. (2000) Caracterización de la captura de tiburón azul (Prionace glauca, Linnaeus, 1758) descargado en Ensenada, Baja California. M.S. thesis, Marine Ecology Program, Centro de Investigación Científica y de Educación Superior de Ensenada, Ensenada, Mexico, 61 pp. Galván-Magaña, F., Nienhuis, H. J. and Klimley, A. P. (1989) Seasonal abundance and feeding habits of sharks of the lower Gulf of California, Mexico. California Fish and Game 75, 74–84. Hernandez, A. and Kempton, W. (2003) Changes in fisheries management in Mexico: Effects on increasing scientific input and public participation. Ocean and Coastal Management 46, 507–526. Holts, D. B., Julian, A., Sosa-Nishizaki, O. and Bartoo, N. (1998) Pelagic shark fisheries along the west coast of the United States and Baja California, Mexico. Fisheries Research 39, 115–125. Macías-Zamora, R., Vidaurri-Sotelo, A. L. and Santana-Hernández, H. (1994) Analysis of the tendency of catch per unit of effort in the Mexican Pacific sailfish fishery. Ciencias Marinas 20, 393–408. Márquez-Farías, J. F. (2002) Tiburones del Golfo de California. In: Sustentabilidad y pesca responsable en México: Evaluación y manejo 1999–2000. Instituto Nacional de la Pesca, Mexico City, Mexico, pp. 237–258. Mendizábal y Oriza, D., Vélez Marín, D., Márquez-Farías, J. F. and Soriano Velásquez, S. R. (2002) Tiburones oceánicos. In: Sustentabilidad y pesca responsable en México: Evaluación y manejo 1999–2000. Instituto Nacional de la Pesca, Mexico City, Mexico, pp. 179–210. SAGARPA (2002) Cancelación de la Norma Oficial Mexicana NOM-029-PESC-2000, pesca responsable de tiburón y especies afines. Especificaciones para su aprovechamiento, publicada el 12 de julio de 2002. In: Diario Oficial, 11 de octubre de 2002, primera sección. Instituto Nacional de la Pesca, Mexico City, Mexico, p. 41. SAGARPA (2004a) Actualización de la carta nacional pesquera. In: Diario Oficial, 15 de marzo de 2004, segunda sección. Instituto Nacional de la Pesca, Mexico City, Mexico, 112 pp.

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SAGARPA (2004b) Anuario estadístico de pesca 2002. www.sagarpa.gob.mx/conapesca/planeacion/ planea.htm. SEMARNAP (2000) Proyecto de Norma Oficial Mexicana NOM-029-PESC-2000, pesca responsable de tiburón y especies afines. Especificaciones para su aprovechamiento. In: Diario Oficial, 11 de octubre de 2000, primera sección. Instituto Nacional de la Pesca, Mexico City, Mexico, p. 41. Soriano-Velásquez, S. R., Solís Nava, A., Ramírez Santiago, C., Cid del Prado Vera, A. and CastilloGéniz, J. L. (2002) Tiburones del Golfo de Tehuantepec. In: Sustentabilidad y pesca responsable en México: Evaluación y manejo 1999–2000. Instituto Nacional de la Pesca, Mexico City, Mexico, pp. 211–236. Sosa-Nishizaki, O. (1998) Historical review of the billfish management in the Mexican Pacific. Ciencias Marinas 24, 95–111.

Part IV

Methods to Improve Understanding of Pelagic Sharks: Demographics, Assessment, and Stock Structure

Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Introduction Fishing is a significant and growing source of mortality for open ocean sharks. Conservation of these species, therefore, will be facilitated by a better understanding of the impact of fishing on their population status and trends, as well as improved knowledge of the constraints imposed by their life-history traits, stock structure, and movements. This section presents new methods of numerical, genetic, and tagging analysis for developing useful tools for the management and conservation of pelagic sharks.

Demography Demographic methods use estimates of the age-specific mortality and fecundity of animals to evaluate a population’s ability to increase over time, with or without mortality caused by fishing. Such methods are useful for open ocean sharks because they do not rely on data from fisheries, which are often lacking or inaccurate (Chapter 31). Sharks tend to grow slowly, mature late, and bear few offspring relative to the teleost fishes (Chapter 3). These life-history traits make elasmobranchs more vulnerable to fisheries, and open ocean sharks are no exception. This part begins with three chapters that employ different assumptions and demographic methods to evaluate the productivity of open ocean shark populations. Chapter 27 uses a probabilistic method that allows for variation in life-history parameters to evaluate the impact of increasing fishing mortality on juvenile and adult life stages. This analysis found that juvenile and adult survival rates (not fecundity) are the most important factors in predicting population growth rates. The biomass that is needed to support the maximum sustainable yield for a population of open ocean sharks is above 50% of the unfished biomass, implying that these sharks are more vulnerable to overfishing than are other pelagic fishes. Chapters 25 and 26 use a demographic method that incorporates density-dependent effects to estimate a population’s “rebound potential,” which is the capacity to rebuild after having been fished at its maximum sustainable yield. Rebound potentials of open ocean sharks were found to be in the midrange for elasmobranchs; pelagic stingrays (Pteroplatytrygon violacea) were the most productive and bigeye threshers (Alopias superciliosus) the least (Chapter 25). Chapter 26 compares open ocean sharks to other sharks and teleosts to evaluate the level of fishing mortality that would yield the maximum sustainable yield, and found that the maximum sustainable fishing mortality rate (relative to the natural mortality rate) was lower for sharks than for teleosts. Furthermore, protecting reproductive females from exploitation allowed the population to sustain higher levels of fishing. Despite their differing assumptions and methodologies, all three of these demographic analyses were consistent in finding that protecting adults is more important than protecting young-of-the-year sharks for rebuilding shark populations, and all three concluded that sustainable catch levels were relatively low.

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Stock structure and movement Little is known about the stock structure of open ocean sharks. To understand the impact of fishing on shark populations, it is necessary to know whether sharks migrate between regions undergoing different levels and types of fishing activity. Studies of genetic population structure can be useful for determining whether there is migration between geographic areas. However, a small number of migrants per generation are sufficient to render two populations genetically indistinguishable. Also, some species exhibit natal philopatry, yet undergo widespread migrations through ocean basins as adults, so that genetic population structure can be found between pupping areas, but not in the open ocean areas where fisheries occur. Thus, genetic methods are only one approach to assessing whether stocks should be considered separate for management purposes. For shortfin makos (Isurus oxyrinchus), mitochondrial DNA analysis indicated a distinct population in the North Atlantic, and some genetic differentiation throughout the world (Chapter 28). Other species of open ocean sharks have not been studied in detail. Genetic methods are also useful for identifying the species of origin of shark products for more informed monitoring and enforcement (Chapter 29). Tagging data indicate that North Atlantic blue sharks (Prionace glauca) comprise a single stock with frequent movement between the eastern and western Atlantic (Chapter 30). They exhibit seasonal segregation by size and sex, with smaller, immature individuals occurring at higher latitudes. Movements revealed in the tagging data are consistent with mating areas in the northwestern North Atlantic and pupping areas in the eastern North Atlantic. Blue sharks also have some exchange between the North and South Atlantic.

Stock assessment The usual approach in assessing the status of a population is to develop a mathematical model of its dynamics and then fit the model to catch and catch-rate data from the relevant fisheries. This method has been applied to open ocean sharks, for example, for porbeagles (Lamna nasus) in the Northwest Atlantic (Chapter 35). For many species, however, catch and catch-rate data are lacking or incomplete, making it necessary to use methods that can adequately account for uncertainty and that use all available information most effectively. In particular, Bayesian methods can be used to incorporate both demographic and fisheries data into an assessment (Chapter 31), so as to calculate the relative credibility of multiple hypotheses about shark biology and population dynamics. This approach facilitates the development of management strategies that can address uncertainties in both life-history data and fisheries catch data. Incorrect assumptions about stock structure and movement can lead to faulty conclusions about the level of fishing that is sustainable in a given region, especially for migratory species like the open ocean sharks. Thus, information about these processes should be incorporated into an assessment. Chapter 32 presents an assessment for school sharks (Galeorhinus galeus) that used tagging data to improve estimates of migration, as well as of historical abundance and fishing mortality rates. Historical tagging data improved the precision of the estimates of stock status and generated more information on migration, both of which were useful in designing management actions.

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Conclusion Open ocean sharks are one of the least-studied groups of large vertebrates. Recent work in life history, genetics, tagging, and numerical analysis has improved our understanding of these species. Despite these advancements, much more research is needed on stock structure and movement, as well as on the impacts of fishing on population dynamics, to facilitate effective management plans for these highly migratory oceanic sharks.

Chapter 25

Intrinsic Rates of Increase in Pelagic Elasmobranchs Susan E. Smith, David W. Au and Christina Show

Abstract Elasmobranch demography is briefly reviewed and intrinsic rebound rates are calculated for 11 selected pelagic species. These rates are compared to those of 22 other shark species calculated by the same method. Rates of population increase for most pelagic species fall within the middle range of the shark productivity spectrum, but some lie near the limits of the entire range, from a low of 1–2% per year for basking shark (Cetorhinus maximus) to a high of 6–10% per year for pelagic stingray (Pteroplatytrygon violacea). All calculated elasmobranch values are low compared to those of most teleosts, especially if a total mortality equaling 1.5 times the instantaneous natural mortality is considered to be the most appropriate for producing maximum sustainable yield in sharks. Key words: demographic analysis, intrinsic rates of increase, population growth rate.

Introduction Demography, developed originally to forecast human population growth, combines ageor stage-specific mortality and natality rates to produce estimates of net reproductive rate, generation time, and per capita instantaneous rate of increase of a population (r). The method is useful for sharks because surplus production modeling or other age-structured analyses are often not feasible for many species for which catch-rate and age data are lacking. Our purpose is to briefly review shark demography and compare rebound potentials of pelagic versus nonpelagic shark species, with rebound ability being a proxy for sensitivity to fishery exploitation. All demographic models used for elasmobranchs are based on the equation developed by Euler (1760) and rediscovered by Lotka (1907). It demonstrates that when age-specific rates of survivorship and fecundity remain constant with time, an age distribution eventually forms where the proportion of the population in each age interval remains constant, and the population then increases at an intrinsic rate r. It is the basic equation of population dynamics; most statistics of population analyses are derived from it. Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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This equation may be written (e.g., Stearns, 1992) w

∑ lx e
rx mx  1

xα

where age at maturity (α), age at last reproduction (w), probability of survival to a given age class (lx), and number of offspring produced by a given age class (mx) are related to the rate of growth (r) of the population. The stable-aged condition is assumed, in which the population grows smoothly and exponentially, and when not growing it is in a stationary condition (r  0). The resulting rate (r) is considered the maximum potential growth rate for a given survival–fecundity schedule. The rate usually (though not always) represents the rate achieved in the absence of crowding, resource competition, or any other built-in compensatory response related to population density. The model is a useful conceptual construct, especially for wide-ranging pelagic sharks that are difficult to sample. A major drawback is the difficulty of obtaining empirical estimates or suitable proxies for the probability of survival to age x. Survival schedules are lacking for most elasmobranchs, thus mortality is usually estimated indirectly and broadly applied, with assumptions made for various age classes or stages. These assumptions usually differ among studies, making comparison of results difficult. Traditional demographic methods of varying complexity have been used to estimate rates of increase for nonpelagic sharks such as spiny dogfish (Squalus acanthias, Squalidae; Jones and Geen, 1977), angel shark (Squatina californica, Squatinidae; Cailliet et al., 1992; Heppell et al., 1999), bonnethead (Sphyrna tiburo, Sphyrnidae; Cortés and Parsons, 1996; Cortés, 1998), and the following carcharhinid sharks: lemon (Negaprion brevirostris; Hoenig and Gruber, 1990; Cortés, 1998), sandbar (Carcharhinus plumbeus; Hoff, 1990; Sminkey and Musick, 1996; Cortés, 1999; Brewster-Geisz and Miller, 2000), blacktip (C. limbatus; Cortés, 1998), dusky (C. obscurus; Cortés, 1998; Simpfendorfer, 1999a), leopard (Triakis semifasciata; Cailliet, 1992; Heppell et al., 1999), Atlantic sharpnose (Rhizoprionodon terraenovae; Cortés, 1995, 1998), and Australian sharpnose (R. taylori; Simpfendorfer, 1999b). In this volume, Cortés (2008) estimates potential rates of increase for eight pelagic sharks under various vital rate scenarios using an age-based probabilistic model that allows assessment of the sensitivity of population growth to proportional mortality increases in young-ofthe-year, juvenile, and adult life stages. A nontraditional method has also been used to compare and rank rates of increase in an array of pelagic and nonpelagic sharks hypothetically exposed to a maximum sustainable level of harvest (Au and Smith, 1997; Smith et al., 1998; Show, 2000; Au et al., 2008). Like traditional methods, it uses the Euler–Lotka equation as its base, but also incorporates concepts of sustainability and population compensation to circumvent the survival schedule problem and other data limitations, and to compare species. The method is used here to estimate the rebound rates of 11 pelagic elasmobranch species. Unlike standard demographic analyses, this method approximates each species’ growth potential for sustaining a given level of harvest, which becomes its potential to increase once fishing is removed.

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Methods The approach of Au and Smith (1997) and Smith et al. (1998) is used to determine the intrinsic rebound potential rZ(MSY) at a total mortality level chosen for maximum sustainable yield. Unlike traditional r values, this method estimates population growth rates for each species at the same population level – about half the virgin population size (Fig. 25.1). A density-dependent feature allows the modeled population to respond to imposed fishing mortality and enables estimation of net juvenile survival.

Estimating the intrinsic rate of increase rZ(MSY) or rebound potential

Intrinsic rate of population increase

As in Au and Smith (1997) and Smith et al. (1998, Equation 3), rZ(MSY) is estimated using age at maturity α, maximum reproductive age w, adult instantaneous natural mortality M, average number of female pups per adult female b, and survival to age at maturity lα. Juvenile survival lα replaces survival to a given age class lx up to age α and is determined by assuming that the total adult mortality Z to be applied is sustainable, and that juvenile survival compensates for any reduced reproductive output resulting from this imposed mortality. The value of rZ(MSY) is then determined by removing fishing mortality and allowing the population to rebound in an unfished state with juvenile survival remaining at the “enhanced” compensatory level. Previously (Smith et al., 1998) the traditional mortality level of ZMSY  2.0M was applied, but here we use it as a comparative upper value. The level ZMSY  1.5M as proposed by Au et al. (2008) is now considered to be the more appropriate maximum estimate for sharks using our method (see also Cortés, 2008). The value of M (or Z in the unfished state) is estimated from maximum age as described by Hoenig (1983; ln M  1.44
0.982 ln w). Among indirect methods, Hoenig produced the most realistic estimate for R. taylori in a study comparing seven indirect methods for estimating M with an empirical method based on catch curve analysis (Simpfendorfer, 1999b). The value of M can also be estimated from body size (Peterson and Wroblewski, 1984). Smith et al. (1998) discussed various caveats in estimating rZ(MSY) using this method. Species A Net production Z(MSY)

Species B

Species C

0.0

0.5

K

Population size (fraction carrying capacity K) Fig. 25.1 Schematic representing r as a decreasing function of population density, with points representing intrinsic rates of increase for species of varying productivities (A being most productive; C being least productive) measured at 0.5 of carrying capacity K.

Intrinsic Rates of Increase in Pelagic Elasmobranchs

291

Choosing and applying life-history parameters Parameters were obtained from the literature and expert sources for 10 pelagic shark stocks and one pelagic stingray as cited in Table 25.1 and as described by Smith et al. (1998). Values of b account for reproductive cycles of more than 1 year. The fecundity adjustment described in Smith et al. (1998) is not applied here. Rebound rates based on parameters from Smith et al. (1998) are presented for 22 other shark species/stocks for comparison: sevengill (Notorynchus cepedianus, Hexanchidae); spiny dogfish (Northeast Pacific and Northwest Atlantic stocks); angel shark; sand tiger (Carcharias taurus, Odontaspididae); white shark (Carcharodon carcharias, Lamnidae); the triakid sharks, school (Galeorhinus galeus), gray smoothhound (Mustelus californicus), brown smoothhound (M. henlei), and leopard; the carcharhinid sharks, gray reef (Carcharhinus amblyrhynchos), Galapagos

Table 25.1 Intrinsic rebound potential estimates for selected pelagic elasmobranch species, listed in order of most productive to least, calculated for ZMSY  1.5M and ZMSY  2.0M. Species/parametersa α (year) w (year)

b

M (year
1) r1.5M (year
1) CV (r1.5M)

r2.0M (year
1) CV (r2.0M) Referencesb

Pelagic stingray (Pteroplatytrygon violacea, Dasyatidae, northeastern Pacific) 3 8 3.0 0.548 0.062 0.091 0.104

0.089

1

Oceanic whitetip (Carcharhinus longimanus, Carcharhinidae, North and South Pacific) 5 22 3.0 0.203 0.039 0.070 0.067

0.070

2

Common thresher (Alopias vulpinus, Alopiidae, northeastern Pacific) 5 25 2.0 0.179 0.037 0.068

0.065

0.068

3

Shortfin mako (Isurus oxyrinchus, Lamnidae, northwestern Atlantic) 6 15 3.1 0.295 0.036 0.092

0.062

0.088

4

Blue shark (Prionace glauca, Carcharhinidae, North Pacific and North Atlantic) 6 20 11.6 0.223 0.035 0.076 0.061

0.076

5, 6, 7

Porbeagle (Lamna nasus, Lamnidae, southwestern Pacific) 8 30 1.9 0.150 0.026

0.072

0.046

0.073

8, 9, 10

Salmon shark (L. ditropis, Lamnidae, northwestern Pacific) 9 25 2.3 0.179 0.024 0.083

0.043

0.082

11, 12

Silky shark (C. falciformis, Carcharhinidae, western Atlantic) 9 25 2.6 0.179 0.025 0.084

0.043

0.082

13

Pelagic thresher (A. pelagicus, Alopiidae, northwestern Pacific) 9 29 1.0 0.155 0.024 0.076

0.043

0.077

14

Bigeye thresher (A. superciliosus, Alopiidae, northwestern Pacific and northeastern Atlantic) 13 20 1.0 0.223 0.016 0.233 0.028 0.203 Basking shark (Cetorhinus maximus, Cetorhinidae, Atlantic) 18 50 1.5 0.091 0.012 0.118

0.018

0.125

15, 16, 17 18, 19

α: female age at maturity; w: maximum reproductive age; b: average number of female pups per adult female annually; M: natural mortality rate; r: intrinsic rebound potential at Z  1.5M, Z  2.0M; CV: coefficient of variation for r1.5M and r2.0M. b Other than cited in Smith et al. (1998), as follows: 1: Henry F. Mollet, September 1999, personal communication, Monterey Bay Aquarium, Monterey, CA; 2: Seki et al. (1998); 3: Smith et al. (2008); 4: Mollet et al. (2000); 5: Cailliet et al. (1983); 6: Tanaka et al. (1990); 7: Nakano and Seki (2002); 8: Aasen (1963); 9: Francis and Stevens (2000); 10: Francis et al. (2008); 11: Tanaka (1980); 12: Goldman and Human (2005); 13: Bonfil et al. (1993); 14: Liu et al. (1999); 15: Moreno and Morón (1992); 16: Chen et al. (1997); 17: Liu et al. (1998); 18: Pauly (1978); 19: Pauly (2002). a

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(C. galapagensis), bull (C. leucas), blacktip, dusky, sandbar, tiger (Galeocerdo cuvier), lemon, Atlantic sharpnose, and whitetip reef (Triaenodon obesus); and the sphyrnid sharks, scalloped hammerhead (Sphyrna lewini) and bonnethead.

Precision We carried out Monte Carlo simulations (n  10,000) of rZ to determine the distribution and coefficient of variation (CV) of each species’ productivity estimates, given combinations of age at maturity α and maximum age w values, adjusting natural mortality M inversely as w varied. Both α and w were presumed to vary 20% about their mean or estimated values, a reasonably conservative estimate of variation in these parameters, which represent average values over the long term. The probability distributions of α and w were assumed to be normal with 20% representing two standard deviations (i.e., CV  10%). Fecundity was held constant. Confidence intervals are calculable from CV and rZ(MSY) (mean) values.

Results Rebound rates among the pelagic sharks examined ranged from a high of 6–10% per year for pelagic stingray to a low of 1–2% per year for basking shark (Table 25.1). All others fell between 2–4% (Z  1.5M) or 3–7% (Z  2.0M) per year. Precision of estimated rZ(MSY) is indicated by listed CVs, which ranged between 0.068 and 0.233 with distributions approximately normal. The basking and bigeye thresher (Alopias superciliosus, Alopiidae) sharks are among the least productive of the 33 elasmobranchs considered, similar to many slow-growing, late-maturing large coastal sharks (Fig. 25.2). The pelagic stingray was among the most productive, similar to small inshore coastal sharks, which are all relatively fast-growing and early to mature. The more productive species had a greater rZ(MSY) range than the less productive species, with rates differing widely under the Z  1.5M and Z  2M mortality conditions, indicating a higher sensitivity to imposed mortality. Differences under the two mortality assumptions ranged from 0.01 (Z  1.5M) to 0.017 (Z  2M) for the least productive spiny dogfish, to 0.079 (Z  1.5M) to 0.139 (Z  2M) for the most productive gray smoothhound. For the pelagic elasmobranchs, the r1.5M values averaged 58% lower than the r2.0M values.

Discussion Most pelagic elasmobranchs are in the midrange of shark productivity, but the range is broader than previously thought. Basking and bigeye thresher sharks rank among the least productive examined to date with this method; both have low reproductive rates and advanced ages at first maturity. Cortés (2008) has also obtained low r values for bigeye thresher using a different demographic method. This late-maturing, long-lived strategy is similar to that of medium to large coastal shark species, and indeed both sharks seem to diverge from the epipelagic shark ecotype with their particular habitat and trophic

Intrinsic Rates of Increase in Pelagic Elasmobranchs

0.0

0.02

0.04

Spiny dogfish (B.C.) Dusky shark Basking shark Sevengill shark Bull shark Scalloped hammerhead Sandbar shark Bigeye thresher Leopard shark School/soupfin shark Spiny dogfish (NW Atlantic) Lemon shark Angel shark White shark Tiger shark Pelagic thresher Silky shark Salmon shark Porbeagle (S. Pacific) Galapagos shark Whitetip reef shark Sand tiger shark (Atlantic) Gray reef shark Blacktip shark Blue shark Shortfin mako shark Common thresher Oceanic whitetip

0.06

0.08

0.10

293

0.12

Productivity comparison among elasmobranchs

MSY mortality level (Z ) 1.5 M

2.0 M

Atlantic sharpnose Bonnethead shark Pelagic stingray Brown smoothhound Gray smoothhound 0.0

0.02

0.04

0.06

0.08

0.10

0.12

MSY

Fig. 25.2 Productivity comparison of pelagic elasmobranchs (in bold) with other shark species. Values for nonpelagic species are taken from Smith et al. (1998) and Au et al. (2008).

specializations. The basking shark is a sluggish, primarily coastal, filter-feeding species (Compagno, 1984). The bigeye thresher can occur near the surface, but generally ranges deeper than other threshers, although it may also enter coastal and even shallow waters (Gruber and Compagno, 1981). According to cited references, parameters for the basking shark are preliminary, but those of the bigeye thresher appear more reliable, except perhaps w may be underestimated. The low w in relation to high α likely caused the relatively high CV value (0.19) for bigeye, but even increasing w to 30 years would have little effect on productivity, which is primarily driven by α. Inexact estimates of w also directly affect estimates of M, a drawback of using Hoenig’s (1983) method, although long-lived species appear least affected by inaccuracies in M (Au et al., 2008).

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The pelagic stingray is one of the most productive elasmobranchs we examined, but its parameters are also preliminary. Little is known of the reproductive periodicity and fecundity of the viviparous rays, such as P. violacea (Neer, 2008). Captive young specimens have been observed to grow rapidly and reach sexual maturity within a few years (H. F. Mollet, personal communication). Results of recent biological studies on this species are provided by Neer (2008), who found that maximum age in the wild may extend to 10 years (or more) based on banding patterns. Pelagic sharks with midrange productivities appear to invest early in somatic growth, delaying sexual maturity and living longer than the more productive small neritic sharks, while being faster-growing, shorter-lived, and earlier to mature than the least productive coastal sharks. Because of their higher productivity, vast ranges, and greater likelihood of seeding from unfished areas, epipelagic sharks may be more resilient to fishing than the slow-growing, late-maturing coastal sharks. But they are also vulnerable to oceanic fisheries, and early life stages of some may be vulnerable to inshore fisheries as well (Smith et al., 1998). Elasmobranch productivity is low compared to that of many teleosts, being more comparable to the productivity of marine mammals (Smith et al., 1998; Au et al., 2008). Additionally, if ZMSY  1.5M is the more appropriate maximum MSY level for determining the intrinsic rebound potential of elasmobranchs (Au et al., 2008), it is considerably lower and the range narrower than previously estimated using this method. Low-productivity species are particularly vulnerable as represented by the flattest yield curve in Fig. 25.1. Even a slight reduction from their production peak can lead to a dangerously depleted condition. The more productive species may be less sensitive to incremental increases in fishing effort, but their faster turnover rates make them more sensitive to changes in total mortality and to factors affecting their vital rates. Although empirical evidence is still needed to determine how much different species and life stages can adjust their survival under different population conditions, demographic analyses can help approximate the productivity potential of elasmobranchs under mortality conditions observed or hypothetically imposed.

Acknowledgments We thank Enric Cortés, Gregor M. Cailliet, Henry F. Mollet, and Malcolm P. Francis for helpful comments and suggestions, and Henry Mollet for providing pelagic stingray input parameters.

References Aasen, O. (1963) Length and growth of the porbeagle (Lamna nasus Bonnaterre) in the northwest Atlantic. Fiskerdirektoratets Skrifter, Serie Havundersøkelser 13(6), 20. Au, D. W. and Smith, S. E. (1997) A demographic method with population density compensation for estimating productivity and yield per recruit of the leopard shark (Triakis semifasciata). Canadian Journal of Fisheries and Aquatic Sciences 54, 415–420.

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Au, D. W., Smith, S. E. and Show, C. (2008) Shark productivity and reproductive protection, and a comparison with teleosts. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Bonfil, R., Mena, R. and de Anda, D. (1993) Biological parameters of commercially exploited silky sharks, Carcharhinus falciformis, from the Campeche Bank, Mexico. In: Conservation Biology of Elasmobranchs (ed. S. Branstetter). NOAA Technical Report NMFS 115. NOAA/NMFS, Silver Spring, MD, pp. 73–86. Brewster-Geisz, K. K. and Miller, T. J. (2000) Management of the sandbar shark, Carcharhinus plumbeus: Implications of a stage-based model. Fishery Bulletin 98, 236–249. Cailliet, G. M. (1992) Demography of the central California population of the leopard shark (Triakis semifasciata). Australian Journal of Marine and Freshwater Research 43, 183–193. Cailliet, G. M., Martin, L. K., Harvey, J. T., Kusher, D. and Welden, B. A. (1983) Preliminary studies on the age and growth of blue, Prionace glauca, common thresher, Alopias vulpinus, and shortfin mako, Isurus oxyrinchus, sharks from California waters. In: Proceedings of the International Workshop on Age Determination of Oceanic Pelagic Fishes: Tunas, Billfishes, and Sharks (eds. E. D. Prince and L. M. Pulos). NOAA Technical Report NMFS 8. NOAA/NMFS, Silver Spring, MD, pp. 179–188. Cailliet, G. M., Mollet, H. F., Pittenger, G. G., Bedford, D. and Natanson, L. J. (1992) Growth and demography of the Pacific angel shark (Squatina californica), based upon tag returns off California. Australian Journal of Marine and Freshwater Research 43, 1313–1330. Chen, C., Liu, K. and Chang, Y. (1997) Reproductive biology of the bigeye thresher shark, Alopias superciliosus (Lowe, 1839) (Chondrichthyes: Alopiidae), in the northwestern Pacific. Ichthyological Research 44, 227–235. Compagno, L. J. V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 2. Carcharhiniformes. FAO Fisheries Synopsis No. 125. FAO, Rome, Italy, pp. 251–655. Cortés, E. (1995) Demographic analysis of the Atlantic sharpnose shark, Rhizoprionodon terraenovae, in the Gulf of Mexico. Fishery Bulletin 93, 57–66. Cortés, E. (1998) Demographic analysis as an aid in shark stock assessment and management. Fisheries Research 39, 199–208. Cortés, E. (1999) A stochastic stage-based population model of the sandbar shark in the western North Atlantic. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 115–126. Cortés, E. (2008) Comparative life history and demography of pelagic sharks. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Cortés, E. and Parsons, G. R. (1996) Comparative demography of two populations of the bonnethead shark (Sphyrna tiburo). Canadian Journal of Fisheries and Aquatic Sciences 53(4), 709–718. Euler, L. (1760) Recherches général sur la mortalité: la multiplication du genre humain. Memoirs of the Academy of Sciences of Berlin 16, 144–164. Francis, M. P. and Stevens, J. D. (2000) Reproduction, embryonic development and growth of the porbeagle shark, Lamna nasus, in the South-west Pacific Ocean. Fishery Bulletin 98, 41–63. Francis, M. P., Natanson, L. J. and Campana, S. E. (2008) The biology and ecology of the porbeagle shark, Lamna nasus. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Goldman, K. J. and Human, B. (2005) Salmon shark, Lamna ditropis Hubbs and Follet, 1947. In: Sharks, Rays and Chimaeras: The Status of the Chondrichthyan Fishes (eds. S. L. Fowler et al.). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 260–262.

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Gruber, S. H. and Compagno, L. J. V. (1981) Taxonomic status and biology of the bigeye thresher, Alopias superciliosus. Fishery Bulletin 79, 617–640. Heppell, S. S., Crowder, L. B. and Menzel, T. R. (1999) Life table analysis of long-lived marine species with implications for conservation and management. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 137–148. Hoenig, J. M. (1983) Empirical use of longevity data to estimate mortality rates. Fishery Bulletin 81, 898–903. Hoenig, J. M. and Gruber, S. H. (1990) Life history patterns in the elasmobranchs: Implications for fisheries management. In: Elasmobranchs As Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries (eds. H. L. Pratt Jr., S. H. Gruber and T. Taniuchi). NOAA Technical Report NMFS 90. NOAA/NMFS, Silver Spring, MD, pp. 1–16. Hoff, T. B. (1990) Conservation and Management of the Western North Atlantic Shark Resource Based on the Life History Strategy Limitations of the Sandbar Shark. Ph.D. thesis, University of Delaware, Newark, DE, 282 pp. Jones, B. C. and Geen, G. H. (1977) Reproduction and embryonic development of spiny dogfish (Squalus acanthias) in the Strait of Georgia, British Columbia. Journal of the Fisheries Research Board of Canada 34, 1286–1292. Liu, K., Chiang, P. and Chen, C. (1998) Age and growth estimates of the bigeye thresher shark, Alopias superciliosus, in northeastern Taiwan waters. Fishery Bulletin 96, 482–491. Liu, K., Chen, C., Liao, T. and Joung, S. (1999) Age, growth, and reproduction of the pelagic thresher shark Alopias pelagicus in the northwestern Pacific. Copeia 1999, 68–74. Lotka, A. J. (1907) Studies on the mode of growth of material aggregates. American Journal of Science 24, 199–216, 375–376. Mollet, H. F., Cliff, G., Pratt Jr., H. L. and Stevens, J. D. (2000) Reproductive parameters of female shortfin mako Isurus oxyrinchus (Rafinesque, 1809) with comments on the embryonic development of lamnoids. Fishery Bulletin 98, 299–318. Moreno, J. A. and Morón, J. (1992) Reproductive biology of the bigeye thresher shark, Alopias superciliosus (Lowe, 1839). Australian Journal of Marine and Freshwater Research 43, 77–86. Nakano, H. and Seki, M. P. (2002) Synopsis of biological data on the blue shark, Prionace glauca Linnaeus. Bulletin of the Fisheries Research Agency 6, 18–55. Neer, J. A. (2008) The biology and ecology of the pelagic stingray, Pteroplatytrygon violacea (Bonaparte, 1832). In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Pauly, D. (1978) A Critique of Some Literature Data on the Growth, Reproduction and Mortality of the Lamnid Shark Cetorhinus maximus (Gunnerus). ICES C.M. 1978: H17. International Council for the Exploration of the Sea, Copenhagen, Denmark, 10 pp. Pauly, D. (2002) Growth and mortality of the basking shark Cetorhinus maximus and their implications for management of whale sharks Rhincodon typus. In: Elasmobranch Biodiversity, Conservation and Management (eds. S. L. Fowler, T. M. Reed and F. A. Dipper). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 199–208. Peterson, I. and Wroblewski, J. S. (1984) Mortality rate of fishes in the pelagic ecosystem. Canadian Journal of Fisheries and Aquatic Sciences 41, 1117–1120. Seki, T., Taniuchi, T., Nakano, H. and Shimizu, M. (1998) Age, growth and reproduction of the oceanic whitetip shark from the Pacific Ocean. Fisheries Science 64, 14–20. Show, C. (2000) Solving for Intrinsic Rebound Potentials with the Solver Program. Administrative Report LJ-00-01. Southwest Fisheries Science Center, NMFS, La Jolla, CA, 12 pp.

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Simpfendorfer, C. A. (1999a) Demographic analysis of the dusky shark fishery in southwestern Australia. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 149–160. Simpfendorfer, C. A. (1999b) Mortality estimates and demographic analysis of the Australian sharpnose shark, Rhizoprionodon taylori, from northern Australia. Fishery Bulletin 97, 978–986. Sminkey, T. R. and Musick, J. A. (1996) Demographic analysis of the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic. Fishery Bulletin 94, 341–347. Smith, S. E., Au, D. W. and Show, C. (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678. Smith, S. E., Rasmussen, R. C., Ramon, D. A. and Cailliet, G. M. (2008) The biology and ecology of thresher sharks (Alopiidae). In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Stearns, S. C. (1992) The Evolution of Life Histories. Oxford University Press, New York. Tanaka, S. (1980) Biological survey of salmon shark, Lamna ditropis, in the western North Pacific Ocean. In: Report of New Shark Resource Exploitation Survey in the Fiscal Year 1979, North Pacific Ocean. Japan Marine Fishery Resource Research Center, Tokyo, Japan, pp. 59–84. Tanaka, S., Cailliet, G. M. and Yudin, K. G. (1990) Differences in growth of the blue shark Prionace glauca: Technique or population? In: Elasmobranchs As Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries (eds. H. L. Pratt Jr., S. H. Gruber and T. Taniuchi). NOAA Technical Report NMFS 90. NOAA/NMFS, Silver Spring, MD, pp. 177–187.

Chapter 26

Shark Productivity and Reproductive Protection, and a Comparison with Teleosts David W. Au, Susan E. Smith and Christina Show

Abstract Intrinsic rates of increase at the population size for maximum sustainable yield (MSY), that is, rebound potentials, are calculated for 27 sharks and 10 large pelagic teleosts after determining the mortalities producing MSY. Those mortalities, Z
1.5M and Z
2.0M, respectively, were derived by linking stock–recruitment and abundance-per-recruit relationships via Lotka’s demographic equation. Rebound potentials ranged from 1% to 14% per year for sharks and from 8% to 34% for billfishes and tunas. Small coastal sharks have productivities similar to those of some large teleosts and could recover from depletion within a decade. The least productive sharks would require as long as four decades. Pelagic sharks have mostly intermediate productivities. Most sharks would suffer population collapse with mortalities around three times the rate of natural mortality. Protecting the first two to three mature ages of the most productive sharks, but up to the first 10 mature ages of the least productive, would ensure enough reproduction to prevent population collapse. Key words: collapse threshold, rebound potential, reproductive protection, shark productivity, population collapse.

Introduction Demographic analysis is a useful tool for studying shark populations, especially for comparing productivities among species or predicting responses to fishing based on lifehistory traits and reproductive potential. Here we review the “intrinsic rebound potential” that Smith et al. (1998) calculated to measure the productivity of sharks, and evaluate how protecting the reproductive potential incorporated in that measure can guard against population collapse. We will show how the mortality rate that produces maximum sustainable yield (MSY) can be determined and will compare productivities among different sharks, and some teleost species. We will also consider the likely bounds of these estimates, the mortality levels at which populations collapse, and the years required for depleted populations to recover. Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Methods Estimating productivity Intrinsic rebound potential measures the productivity of a population as it hypothetically rebounds from the size producing MSY, and hence estimates the productivity producing that yield (Au and Smith, 1997; Smith et al., 1998). It is a solution of Lotka’s (1907) demographic equation, utilizing the concept that through density-dependent compensation every adult mortality rate up to some maximum can be sustained. This allows direct estimation of pre-adult survival, and thus circumvents a major difficulty of conventional demographics. To review, the Euler–Lotka (Lotka’s) equation in discrete form is w

∑ lx erx mx
1

(26.1)

x
α

where α
female age at first reproduction, w
last reproducing age, lx
survival to age x, mx
fecundity at age x (female offspring), and r
intrinsic rate of increase. After substituting lαeM(xα) for lx (where lα
survival to maturity and M
instantaneous rate of natural mortality) and average fecundity b for mx, completing the summation then gives e( M r )  lα berα [1  e( M r )( wα1) ]
1

(26.2)

which is equivalent to Leslie’s (1966) expression when w is sufficiently large. The net preadult survival lα
lα,Z that makes an increased mortality Z (
M  fishing mortality F) sustainable (r
0) is determined from Equation (26.2) set with M
Z and r
0. If fishing mortality is now removed (Z becomes M), the population under survival lα,Z will rebound at a certain productivity rate rZ (with the stable-aged distribution achieved), again as found from Equation (26.2) accordingly specified (the “rebound” transforms catch mortality into its population growth equivalent).

Parameters of rebound potential Age α and mortality M Average age at first maturity α and natural mortality M were taken from the literature, where M was often calculated from maximum age w: ln M
1.44–0.982 ln w (Hoenig, 1983; see Table 26.1). That equation is a variant of the exact relationship analytically derived by Xiao (2001).

Fecundity In determining lα,Z, average fecundity is used directly, but for rZ its effect is as the ratio of fecundity during the rebound phase (when average fecundity is higher from higher adult survival) to fecundity during the fished phase (large females culled).* So by assuming a b-ratio, rebound potential can be estimated even for species whose fecundity schedules are poorly This comes from assuming compensation in l,Z alone makes r
0 possible; however, allowing the compensation to be within the product (l,Zb), instead, would still give the same resulting rZ. *

300

Sharks of the Open Ocean

Table 26.1 Intrinsic rebound potentials (rZ) and doubling times (TD) for (a) 10 sharks (with Z
1.5M) and (b) 10 pelagic teleosts (with Z
2.0M) at two fecundity b-ratios (1.00, 1.25). Parameters*

b-ratio 1.00 TD (year)

rZ (year1)

TD (year)

Gray smoothhound (Mustelus californicus, Triakidae) 2 12 1.6 0.368 0.079

5.8

0.141

3.3

Bonnethead (Sphyrna tiburo, Sphyrnidae) 3 12 4.5 0.368

α (year)

w (year)

b (F/F)

M (year1)

rZ (year1)

b-ratio 1.25

(a) Sharks

7.5

0.110

4.2

Sharpnose, Atlantic (Rhizoprionodon terraenovae, Carcharhinidae) 4 10 2.5 0.440 0.050

0.062

9.2

0.092

5.0

Common thresher (Alopias vulpinus, Alopiidae) 5 19 2.0 0.234

0.040

11.6

0.069

6.7

Blue (Prionace glauca, Carcharhinidae) 6 20 11.6 0.223

0.035

13.2

0.060

7.7

Mako (Isurus oxyrinchus, Lamnidae) 7 28 4.0 0.160

0.029

15.9

0.049

9.4

White (Carcharodon carcharias, Lamnidae) 9 36 3.5 0.126

0.023

20.1

0.038

12.2

Leopard (Triakis semifasciata, Triakidae) 13 30 6.0 0.150

0.018

25.7

0.031

14.9

Bull (Carcharhinus leucas, Carcharhinidae) 15 27 1.8 0.166

0.015

30.8

0.027

17.1

46.2

0.016

28.9

Spiny dogfish, British Columbia (Squalus acanthias, Squalidae) 25 70 3.6 0.065 0.010 (b) Billfishes and Tunas Skipjack tuna (Katsuwonus pelamis, Scombridae) 1 5 1.500

0.160

2.9

0.344

1.3

Yellowfin tuna (Thunnus albacares, Scombridae) 2.5 8 0.900

0.109

4.2

0.182

2.5

Bigeye tuna (Thunnus obesus, Scombridae) 3 10 0.400

0.104

4.4

0.156

3.0

Sailfish (Istiophorus platypterus, Istiophoridae) 3 8 0.530

0.104

4.4

0.160

2.9

Striped marlin (Tetrapturus audax, Istiophoridae) 4 9 0.470

0.082

5.6

0.126

3.7

Blue marlin (Makaira nigricans, Istiophoridae) 4 11 0.380

0.084

5.5

0.125

3.7

Albacore tuna (Thunnus alalunga, Scombridae) 4.5 12 0.300

0.074

6.2

0.110

4.2

Bluefin tuna, northern (Thunnus orientalis, Scombridae) 5 20 0.250 0.071

6.5

0.101

4.6

Swordfish (Xiphias gladius, Xiphiidae) 5 20 0.210

0.067

6.9

0.096

4.8

Bluefin tuna, southern (Thunnus maccoyii, Scombridae) 6 20 0.250 0.062

7.5

0.089

5.2

Life-history parameters for sharks are as listed by Smith et al. (1998). α: female age at first reproduction; w: last reproducing age; b: fecundity as female pups per female (F/F); and M: instantaneous rate of natural mortality. Parameters for tunas are as listed by Shomura et al. (1995); for billfishes as listed by Au (1998). *

Shark Productivity and Reproductive Protection

301

known. The b-ratios 1.00 and 1.25 were used, for up to a 25% increase in fecundity as per Smith et al. (1998). (Rebound potentials for pelagic sharks, using population parameters updated from those used here, are presented in Smith et al. (2008). Actual annual rates of increase are estimated for pelagic sharks by Cortés (2008), also with updated parameters, including age survival estimates.)

Population size for MSY Rebound potential is determined for the stock size (S) producing MSY, that is, the SMSY resulting from ZMSY. The linkage to mortality requires a stock–recruitment (S–R) relationship, and we use the normalized Beverton–Holt (BH) S–R model that is appropriate for most marine fishes (Kimura, 1988). In this form, both R and S are in the same relative units. Also, the locus of MSY (
maximum surplus R) forms a diagonal from the upper left

0.4

0.6

0.8

Stock and mortality 1.0

1

2

3

4

5

6

M

0.8

1.0 0.8

SY

Fractional recruitment (R)

0.2

0.6

0.6 S–R

0.4

0.4

0.2

0.2 R/S 0.0 0.0

0.2 0.4 0.6 0.8 Relative stock size (S)

1

1.0

2 3 4 5 6 Mortality Z (in M-multiples)

Fractional stock (SZ /SM)

Stock and recruitment 0.0 1.0

0.0

(a) 0.4

0.6

0.8

Stock and mortality 1.0

1

2

3

4

5

6

1.0 0.8

SY

0.8

0.2 M

Fractional recruitment (R)

0.0 1.0

0.6

0.6

0.4

0.4

0.2

0.2

0.0 0.0

0.4 0.6 0.8 0.2 Relative stock size (S)

1

1.0

2

3

4

5

6

Fractional stock (SZ /SM)

Stock and recruitment

0.0

Mortality Z (in M-multiples) (b)

Fig. 26.1 The procedure, shown diagrammatically, for estimating the mortality ZMSY from an estimate of relative stock size SMSY (arrows indicate translation process for (a) sharks and (b) teleosts). The stock–recruitment (S–R) curve and recruitment–stock (R/S) slope line (left panels) are labeled in the upper left diagram of the normalized BH relationship. SZ/SM curves (right panels) are composites for the species included.

302

Sharks of the Open Ocean

corner of the S–R diagram to the point (0.5, 0.5) on its 1:1 diagonal (Fig. 26.1, left panels). We define R as individuals reaching age α. SMSY is likely to lie within the range 0.2–0.5 of the unfished population size (S0) (Shepherd, 1982). In contrast to certain groundfishes whose stock-independent recruitment gives MSYs at 0.2–0.3S0 (Clark, 1993), the BH S–R model would predict the SMSY for sharks to approach the limiting 0.5S0 (giving zero surplus R) because of their proportional S–R relationship (Holden, 1974). But Thompson (1992) found from theoretical study that SMSY of species like sharks should be from about 0.30 to a maximum 0.37S0, the latter when recruitment is directly proportional to parental stock size. Because others (e.g., Restrepo et al., 1998) have suggested SMSY  0.5S0 for such fishes (which would require some other S–R model), we use Thompson’s theoretical upper limit, rounded to 0.4S0, as the lower bound of SMSY for sharks, the upper bound being the limiting 0.5S0 (but see Cortés, 2008, for still higher SMSY from a relationship to per capita increase per generation). We use SMSY
0.4S0 as the most optimistic estimate of the resilience of sharks. Billfishes and tunas should have smaller SMSY, for they are fast-growing, fecund, and productive, with M relatively high (Table 26.1) and R and S largely independent (e.g., IATTC, 1999, Fig. 43). We therefore place their SMSY at an intermediate 0.3–0.4S0 (between sharks and groundfishes).

Mortality Z for MSY This mortality is derived by linking the above estimates of SMSY to abundance-per-recruit as determined by mortality Z. It can be shown that diagonals drawn from the origin on the S–R diagram represent particular solutions to the demographic equation. Thus if a population produces MSY at stock size SMSY, its S–R curve must intersect the diagram’s MSY locus where it is defined by that SMSY, where the diagonal of slope RMSY/SMSY defining that condition (now with r
0) also intersects the locus (Fig. 26.1, left panels; first bend of up-arrows). The inverse of that RMSY/SMSY slope equates to standing adult stock size per recruit, which is SZ/SM, the spawning stock per recruit (SSR) ratio [(1eZλ)/Z]/[(1eMλ)/M] (where λ
adult life span) (cf. Goodyear’s (1993) spawning potential ratio); it provides for finding ZMSY. SSRs were calculated for different types of sharks (small coastal, pelagic, medium-to-large coastal) and for the large pelagic teleosts (swordfish, marlins, tunas) and depicted as curves determined by Z (Fig. 26.1, right panels). By graphical solution, SMSY is transformed to ZMSY via the RMSY/SMSY diagonal on the S–R diagram and its demographic equivalent, SSR.

Reproductive protection against collapse and time for recovery To determine the value of protecting reproducing adults, we calculated minimum reproductive output for sustaining maximal levels of exploitation. This minimum is obtained at the collapse threshold where productivity is highest and the sustainable mortality maximal at Zτ (Mace and Sissenwine, 1993). An age at fishery entry tc (α  tc  w) in an expanded Equation (26.2) set at that threshold defines this minimum output that prevents collapse while allowing mortality Zτ  Zτ upon the older, still fished ages. The maximum tc is tc max, beyond which there can be 100% exploitation because then the protected unfished age classes alone sustain the population. Two steps lead to solutions: (1) Set r in Equation (26.2) to its maximum value rτ (twice the rZ for MSY, as in the logistic model,

Shark Productivity and Reproductive Protection

303

to allow the largest compensation), and then solve for the maximum pre-adult survival (lα,Z)max; (2) use (lα,Z)max in the expanded Equation (26.2) and solve for combinations of collapse threshold tc and Zτ, and for tc max, with r
0 (for just sustainable fishing) and b-ratio 1.00 (to be conservative). The Zτ are expressed as rates of exploitation Eτ [
(F/ Zτ)(1  exp(Zτ))] varying from 0 to 1.00. To evaluate recovery times after near collapse, we determined doubling times TD for populations depleted to 50% of their MSY-producing sizes. Their rZ, which is then 50% larger (1.5 times) than at MSY (again from the logistic model), is assumed to not change during recovery. Thus we calculated TD
[ln(2)]/1.5rZ as the recovery time for return to the MSY condition.

Results The mortality corresponding to MSY Our estimate of ZMSY is 1.5M for sharks and 2.0M for the pelagic teleosts, from translating estimates of SMSY (see arrow flow in Fig. 26.1). The minimal SMSY for sharks, estimated as 0.40S0, produced an intersection of the MSY locus at (0.40, 0.60) on the S–R plot (Fig. 26.1(a), left panel), which defined a recruitment–stock (R/S) diagonal of slope 0.60/0.40 through that point. This slope’s inverse value, 0.67, is the abundanceper-recruit ratio SSR, as read off the top of the diagram at the diagonal’s intersection. Value 0.67 maps onto the SSR (or SZ /SM) versus Z plot via the 1:1 diagonal (Fig. 26.1(a), right panel), and its intersection with the curve defines its corresponding Z (in multiples of M). Thus the ZMSY for sharks is about 1.5M, an upper bound as derived here. Similarly, it is seen that the median billfish/tuna ZMSY is about 2M, which is the traditionally used value for teleosts (Fig. 26.1(b)).

Productivities: sharks and teleosts The Z-standardized (Z
1.5M, 2.0M) rebound potentials (Table 26.1) are strongly determined by age at maturity α and are plotted accordingly for comparison (Fig. 26.2, with 17 other sharks recalculated from Smith et al., 1998). Most pelagic sharks have r1.5M productivities in the 0.04–0.06 year1 range (e.g., thresher, Alopias vulpinus, Alopiidae), while some small, short-lived coastal sharks, with productivities greater than 0.07 and up to 0.14 year1, may be as productive per capita as some billfishes and tunas. Short-lived tropical tunas (e.g., yellowfin, Thunnus albacares, Scombridae) have r2M values at least three times greater than the r1.5M of the medium-to-large coastal sharks and approximately twice that of the most productive, small coastal sharks. For perspective, Murphy’s (1967) classic r
0.338 for the California sardine (Sardinops sagax, Clupeidae) is shown, a productivity level apparently achievable by the skipjack tuna (Katsuwonus pelamis, Scombridae). How these rZ values are specifically affected by the Z and b-ratios assumed in their determination helps establish their likely bounds (Fig. 26.3). Thus considering likely ranges and interactions of those parameters (higher Z/lower b-ratio of small species; lower Z/higher b-ratio of large species), productivities from about 0.01 to 0.14 year1 would seem likely among sharks as a group. Note that the rZ of the low-productivity sharks (e.g., spiny dogfish,

304

Sharks of the Open Ocean

0.50 0.40

38

0.30 0.20 Intrinsic rebound potential (rz)

28. Skipjack tuna 29. Yellowfin tuna 30. Bigeye tuna 31. Albacore 32. North bluefin tuna 33. South bluefin tuna 34. Swordfish 35. Blue marlin 36. Striped marlin 37. Sailfish 38. Sardine

28

29 30

37 35 36 31 34 32

0.10

33

1

0.08

2

0.06

8

3 4

0.04

5

6

0.02

7 10 11

9 12

15. Tiger 16. White 17. Angel 18. Lemon 19. Spiny dogfish (northwestern Atlantic) 20. School/soupfin 21. Leopard 22. Sandbar 23. Scalloped hammerhead 24. Bull 25. Sevengill 26. Dusky 27. Spiny dogfish (BC)

16 15 17 18 20 21 19

22

23

1. Gray smoothhound 2. Brown smoothhound 3. Bonnethead 4. Sharpnose 5. Common thresher 6. Oceanic whitetip 7. Blue 8. Blacktip 9. Gray reef 10. Sand tiger 11. Mako 12. Whitetip reef 13. Galapagos 14. Silky

24 25

13 14

26 27

0.01

0

5

10 15 Age at maturity (a)

20

25

Fig. 26.2 The relationship of rebound potential rZ to age at maturity α for selected sharks (numbered 1–27) and teleosts (numbered 28–38). The rZ are represented as ranges delimited by rZ calculated with b-ratio 1.25 and 1.00, respectively (with Z
1.5M for sharks and 2.0M for the pelagic teleosts). The estimate for sardine productivity is from Murphy (1967) (solid circle). Ten of the sharks shown are from Table 26.1; the other 17 are recalculated from Smith et al. (1998), using Z
1.5M. Note that the y-axis is log scale.

Squalus acanthias, Squalidae) are relatively unaffected by the ZMSY and b-ratio chosen (their response curves are nearly flat).

Reproductive protection against collapse and recovery times from depletion Without protection of reproducing females, Eτ
Eτ, the basic collapse threshold exploitation. The equivalent Zτ, as M multiples, averaged 2.2M and 4.1M among the sharks of Fig. 26.2, for b-ratio 1.00 and 1.25, respectively. The median of these collapse threshold mortalities, about 3M, is to be compared with the Z
1.5M estimated for MSY. By allowing females a few reproductive seasons before exploitation begins, there can be substantial protection against population collapse, at least for the more productive sharks (Table 26.2). Thus giving females three years of pupping protection (column “3”) would be enough to ensure against collapse of the more productive small coastal species (Eτ becoming 1.00, i.e., the exploited ages become completely expendable (age tc max being surpassed)), and would substantially protect pelagic species like the thresher (Eτ becoming 0.85). This level of reproductive protection is the least needed to save populations when collapse-producing exploitation cannot be prevented.

Shark Productivity and Reproductive Protection

305

0.20

b-ratio
1.00

Productivity rz

0.15

und

thho

moo

s Gray

0.10

0.05

d ethea Bonn se o Sharpn er n thresh Commo Mako White Bull

Spiny dogfish (BC)

0.00 1.0

1.1

1.2

1.3

1.4

1.5

1.6

1.7

1.8

1.9

2.0

0.20 und

thho

moo

s Gray

Productivity rz

d

ethea

b-ratio
1.25

0.15

Bonn

ose

Sharpn

er

n thresh

0.10

Commo

Mako White Bull Spiny dogfish (BC)

0.05

0.00 1.0

1.1

1.2

1.3

1.4 1.5 1.6 1.7 Total mortality (as Z/M)

1.8

1.9

2.0

Fig. 26.3 Responses of the rebound potential statistic rZ among eight representative sharks to total mortality Z (as M multiples) and to unadjusted (1.00b) and adjusted (1.25b) fecundity.

Table 26.2 Increase in maximum (collapse threshold) exploitation rates (Eτ) for 10 sharks according to the number of times adult females are allowed to reproduce before being fished (through raising fishery-entry age above maturity age). Extending the protection past age tc max makes the remaining age classes completely expendable (Eτ
1.00), thus ensuring against collapse under any exploitation rate (age in years and Eτ per year). Species

Gray smoothhound Bonnethead Sharpnose, Atlantic Common thresher Blue Mako White Leopard Bull Spiny dogfish, BC

Sustainable exploitation rate Eτ when there are 1, 2, …, 10 pupping seasons before first exploitation α-age

1

2

3

2 3 4 5 6 7 9 13 15 25

0.31 0.32 0.36 0.22 0.21 0.16 0.13 0.15 0.16 0.07

0.74 0.76 1.00 0.38 0.35 0.23 0.17 0.21 0.24 0.08

1.00 1.00 0.85 0.74 0.36 0.24 0.32 0.38 0.10

4

1.00 1.00 0.70 0.36 0.56 0.76 0.11

5

1.00 0.67 1.00 1.00 0.14

6

7

8

9

10

0.48

3.2 4.1 4.9 7.1 8.2 10.3 13.4 16.6 18.2 1.00 34.0

1.00

0.17

0.22

0.31

tc max

306

Sharks of the Open Ocean

Recovery (doubling) times for depleted shark populations ranged from 3 to 46 years (Table 26.1). Considering TD under both b-ratios, it is clear that the small coastal sharks with rebound potentials around 0.05 or higher (smoothhounds) should recover within a decade (like the teleosts), as might some of the oceanic-pelagic species (e.g., blue, Prionace glauca, Carcharhinidae). However, sharks with potentials less than 0.03, mainly the medium-tolarge coastal species, would require two to four decades to return to the MSY condition.

Discussion Sharks should be managed with emphasis on maintaining healthy reserves of reproducing adults, because catches in excess of annual production rates (
er  1) are easily taken. Raising fishery-entry ages to balance higher exploitation E is a way to obtain the reproductive protection. Thus Holden (1968) determined the lengths at fishery entry for keeping recruitment constant (r
0) among spiny dogfish under different mortalities, and Smith and Abramson (1990) calculated replenishment (net reproductive) rates from combinations of age at entry and mortality for showing when yield per recruit for the leopard shark (Triakis semifasciata, Triakidae) would be unsustainable. Similarly, Au and Smith (1997) adjusted yield per recruit for that shark for reduction in recruitment from exploitation, though in using the rZ-derived productivity–stock rather than the recruitment–stock relationship, they overestimated the decline by 14% at SMSY. Our calculations of the maximum exploitation rates made sustainable by raising age at entry make clear the value of the first few mature age classes in providing necessary reproductive output. Even the most productive sharks require at least three years of protected reproduction to ensure against collapse from extreme exploitation. Such protection might often not be practical, but still is part of the more general concept of protecting reproductive value in populations (MacArthur, 1960). As shown by demographic elasticity analysis of long-lived animals (Cortés, 1999, 2002; Heppell et al., 1999), population growth is enhanced most by protecting those juveniles, subadults, and young adults that are still relatively abundant and with high reproductive potential (having survived the high-mortality years). Protecting pupping females should be a high priority for sustainable management of pelagic sharks, since any pregnant female is most reproductively valuable at the start of the pupping season, having survived all mortality sources up to that time and parturition being imminent.

Acknowledgments For constructive comments, we thank Drs. George Watters, Gregor Cailliet, Enric Cortés, Paul Crone, Malcolm Francis, and Yongshun Xiao.

References Au, D. W. (1998) Protecting the reproductive value of swordfish and other billfishes. In: Biology and Fisheries of Swordfish, Xiphias gladius (eds. I. Barrett, O. Sosa-Nishizaki and N. Bartoo). NOAA Technical Report NMFS 142. NOAA/NMFS, Silver Spring, MD, pp. 219–225.

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Au, D. W. and Smith, S. E. (1997) A demographic method with population density compensation for estimating productivity and yield per recruit of the leopard shark (Triakis semifasciata). Canadian Journal of Fisheries and Aquatic Sciences 54, 415–420. Clark, W. G. (1993) The effect of recruitment variability on the choice of a target level of spawning biomass per recruit. In: Proceedings of the International Symposium on Management Strategies for Exploited Fish Populations (eds. G. Kruse et al.). Report AK-SG-93-02. Alaska Sea Grant College Program, Fairbanks, AK, pp. 233–246. Cortés, E. (1999) A stochastic stage-based population model of the sandbar shark in the western North Atlantic. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 115–126. Cortés, E. (2002) Incorporating uncertainty into demographic modeling: Application to shark populations and their conservation. Conservation Biology 16, 1048–1062. Cortés, E. (2008) Comparative life history and demography of pelagic sharks. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Goodyear, C. P. (1993) Spawning stock biomass per recruit in fisheries management: Foundation and current use. In: Risk Evaluation and Biological Reference Points for Fisheries Management (eds. S. J. Smith, J. J. Hunt and D. Rivard). NRC Research Press, Ottawa, Ontario, Canada, pp. 67–81. Heppell, S. S., Crowder, L. B. and Menzel, T. R. (1999) Life table analysis of long-lived marine species with implications for conservation and management. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 137–148. Hoenig, J. M. (1983) Empirical use of longevity data to estimate mortality rates. Fishery Bulletin 81, 898–903. Holden, M. J. (1968) The rational exploitation of the Scottish–Norwegian stock of spurdogs (Squalus acanthias L.). Fisheries Investigations, London, Series 2 25(8), 27 pp. Holden, M. J. (1974) Problems in the rational exploitation of elasmobranch populations and some suggestions. In: Sea Fisheries Research (ed. F. R. Harden Jones). Wiley, New York, pp. 117–137. IATTC (1999) 1997 Annual Report of the Inter-American Tropical Tuna Commission. IATTC, La Jolla, CA. Kimura, D. K. (1988) Stock–recruitment curves as used in the stock-reduction analysis model. Journal du Conseil International pour l’Exploration de la Mer 44, 253–258. Leslie, P. H. (1966) The intrinsic rate of increase and overlap of successive generations in a population of guillemots (Uria aalge Pont.). Journal of Animal Ecology 35, 291–301. Lotka, A. J. (1907) Studies on the mode of growth of material aggregates. American Journal of Science, Series 4 24, 199–216. MacArthur, R. H. (1960) On the relation between reproductive value and optimal predation. Proceedings of the National Academy of Sciences 46, 143–145. Mace, P. M. and Sissenwine, M. P. (1993) How much spawning per recruit is enough? In: Risk Evaluation and Biological Reference Points for Fisheries Management (eds. S. J. Smith, J. J. Hunt and D. Rivard). NRC Research Press, Ottawa, Ontario, Canada, pp. 101–118. Murphy, G. I. (1967) Vital statistics of the Pacific sardine (Sardinops caerulea) and the population consequences. Ecology 48, 731–736. Restrepo, V. R., Thompson, G. G., Mace, P. M., et al. (1998) Technical Guidance on the Use of Precautionary Approaches to Implementing National Standard 1 of the Magnuson-Stevens Fishery Conservation and Management Act. NOAA Technical Memorandum NMFS-F/SPO-31. NOAA/NMFS, Silver Spring, MD, 54 pp. Shepherd, J. G. (1982) A family of general production curves for exploited populations. Mathematical Biosciences 59, 77–93.

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Shomura, R. S., Majkowski, J. and Harman, R. F. (eds.) (1995) Summary Report of the Second FAO Expert Consultation on Interactions of Pacific Tuna Fisheries, Shimizu, Japan, 23–31 January. FAO Fisheries Report No. 520. FAO, Rome, Italy, Table 2. Smith, S. E. and Abramson, N. J. (1990) Leopard shark Triakis semifasciata distribution, mortality rate, yield, and stock replenishment estimates based on a tagging study in San Francisco Bay. Fishery Bulletin 88, 371–381. Smith, S. E., Au, D. W. and Show, C. (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678. Smith, S. E., Au, D. W. and Show C. (2008) Intrinsic rates of increase in pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Thompson, G. G. (1992) Management advice from a simple dynamic pool model. Fisheries Bulletin 90, 552–560. Xiao, Y. (2001) Formulae for calculating the instantaneous rate of natural mortality of animals from its surrogates. Mathematical and Computer Modelling 33, 783–792.

Chapter 27

Comparative Life History and Demography of Pelagic Sharks Enric Cortés

Abstract Pelagic shark species exhibit differences in life-history traits related to body size, reproduction, age, and growth. These differences are ultimately reflected in their population statistics and dynamics, and the capacity of each individual species to withstand exploitation. Uncertainty associated with age at maturity, longevity, fertility, and natural mortality was incorporated through Monte Carlo simulation to estimate population growth rates (λ) and generation times (T) for eight species of pelagic sharks for which all that information was available. Age-based matrix elasticities (proportional sensitivities) were calculated to help identify the most vulnerable life stages for these species. By determining the relative position of the inflection point of population growth curves (R), it is postulated that the pelagic shark species analyzed reach maximum sustainable yield at or above 50% of their carrying capacity (K). A principal component analysis of five life-history traits yielded groupings that corresponded well with species having similar population growth rates, thus providing a good initial indication of their relative ability to compensate for exploitation. The blue shark (Prionace glauca) is the most productive species, with high fecundity and an inflection point near 50% of K, whereas two of the three Alopias species and the shortfin mako (Isurus oxyrinchus) are the least productive pelagic sharks, with very low fecundity and inflection points that are probably very near K. Elasticity analysis indicated that in all species juvenile survival elasticity was the highest, followed by adult survival elasticity, whereas fertility or age-0 elasticity was low. Although caution should be exercised when making conservation and management recommendations based only on this approach, results indicate that protection should focus mainly on juveniles and also adults rather than age-0 individuals. Given the biology of these pelagic species, it is hardly surprising that recovery to preexploitation levels after intensive fishing will be very slow. Key words: demographic models, density dependence, elasticity analysis, matrix population models, maximum sustainable yield, pelagic sharks.

Introduction Little is known of the demography and dynamics of populations of pelagic shark species. Demographic analyses of shark populations typically have used deterministic life tables and limited sensitivity analyses to estimate intrinsic rates of increase and to assess exploitation Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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potential. Using a modified demographic technique based on density dependence considerations, Smith et al. (1998) estimated intrinsic rebound potentials for a number of shark species, and Smith et al. (2008a) calculated the potentials of 10 pelagic sharks and the pelagic stingray and compared these with 22 other shark species. Mollet and Cailliet (2002) applied a stage-based matrix population model to the pelagic thresher (Alopias pelagicus, Alopiidae). Uncertainty in vital rates has not been incorporated into demographic population models of sharks in general, except for Cortés (1999, 2002), who used Monte Carlo simulation in a stage-based analysis of the sandbar shark (Carcharhinus plumbeus, Carcharhinidae) and in age-based population models for 41 shark populations – including the pelagic species analyzed here. Elasticities (proportional sensitivities; De Kroon et al., 1986) for pelagic sharks were only calculated in the studies by Cortés (2002) and Mollet and Cailliet (2002). One problem associated with the use of deterministic life tables, mean-matrix projections, and deterministic matrix element elasticities is that these approaches do not take account of the full range of natural variability or address the uncertainty in estimates of vital rates for a particular species. Uncritical use of conclusions derived from deterministic population models is potentially dangerous because it can lead to inappropriate conservation measures and management actions (Benton and Grant, 1999). Randomization procedures, such as stage simulation analysis (Wisdom et al., 2000), have been proposed to circumvent the shortcomings of deterministic approaches. With randomization – a form of Monte Carlo simulation – population growth rates (λ), elasticities, and other population parameters of interest can be evaluated across a wide range of vital rates. The relative position of the inflection point of population growth curves or the corresponding peak in production curves, that is, the fraction of the carrying capacity (K) at which the maximum production occurs, is known to vary along a continuum across animal species (Fowler, 1981a, 1988). Very productive commercial fish species are thought to reach the inflection point at a low fraction of K, whereas some large mammals are believed to reach the inflection point at population levels well above 0.5K (Fowler, 1981b, 1987). No studies have investigated this aspect of population dynamics in sharks. In view of the dearth of information on comparative life-history traits and demography of pelagic sharks, the need for incorporating uncertainty in estimates of vital rates into population models, and the lack of information on the position of the inflection point of population growth curves of sharks, this chapter answers the following questions relative to pelagic shark species: (1) Do pelagic shark species exhibit differences in life-history traits that may be ultimately reflected in their population dynamics and capacity to withstand exploitation? (2) How does uncertainty in demographic traits applied consistently to all species affect estimates of population growth rates and generation times on a relative scale? (3) What vital rates exhibit the highest elasticities? and (4) At what fraction of their theoretical carrying capacity are pelagic shark species estimated to reach the maximum sustainable yield (MSY)?

Methods Analysis of differences in life-history traits among species A principal component analysis (PCA) of three observed (maximum adult female body length, offspring length, mean annual fecundity) and two estimated (growth coefficient

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from the von Bertalanffy growth function, k, and empirical maximum age) life-history traits was used to analyze differences among eight species of pelagic sharks. The following populations, for which information on all five traits was available from published sources at the time of this writing, were used in the analysis: pelagic thresher and bigeye thresher (Alopias superciliosus) from the northwestern Pacific, thresher shark (A. vulpinus) from the northeastern Pacific, porbeagle (Lamna nasus, Lamnidae) from the northwestern Atlantic, silky shark (Carcharhinus falciformis, Carcharhinidae) from the southern Gulf of Mexico, oceanic whitetip shark (C. longimanus, Carcharhinidae) from the central and western Pacific supplemented with data from the southwestern equatorial Atlantic, blue shark (Prionace glauca, Carcharhinidae) from the North Atlantic, and shortfin mako (Isurus oxyrinchus, Lamnidae) from the northwestern Atlantic (Table 27.1). To further examine similarities among species, the scores of the first three components of the PCA were used in a hierarchical cluster analysis with a Euclidean distance metric and single linkage method (Unistat Statistical Package v. 4.53, Unistat Ltd., London, UK).

Estimation of population parameters and elasticities Age-structured life tables and Leslie matrices based on a life cycle with reproduction first and then survival (Ebert, 1999, p. 83) for a yearly time-step applied only to females were used to model the demography of the eight species of pelagic sharks. Monte Carlo simulation was used to incorporate uncertainty in demographic parameters and generate estimates of population growth rates, generation times, and elasticities for a large set of life tables/Leslie matrices that spanned a wide range of possible values. Age at maturity, maximum age, and age-specific fecundity and survivorship were randomly selected from statistical distributions assumed to describe these demographic parameters. Age at maturity was represented by a triangular distribution (Table 27.1; and see Fig. 1 in Cortés, 2002). Generally a single value (obtained by back-transforming the length at which a female first becomes mature, or in other cases, the length at which 50% of the population matures, into age through a von Bertalanffy growth function) was reported in the literature and set as the likeliest value, with the lower and upper bounds obtained using ⫾1 year as an approximation; if a range of ages was reported, the midpoint was used as the likeliest value and the range was used to bound the distribution. Age at first reproduction was set to 1 year after age at maturity. Maximum age was represented by a linearly decreasing distribution scaled to a total relative probability of 1. The likeliest value used was the highest empirical value of longevity reported in the literature, while the unlikeliest value was obtained by arbitrarily adding 30% to that value. The probability of survival at age was estimated through six indirect life-history methods that have been described extensively elsewhere (Cortés, 2002, and references therein). Four of these methods rely largely on parameter estimates derived from the von Bertalanffy growth function, one on knowledge of longevity, and one on weight information to estimate natural mortality. The lower and higher estimates from the six methods were used to bound a linearly increasing distribution scaled to a total relative probability of 1. The likeliest value in this distribution was assigned to the highest estimate of survival, while the unlikeliest value was the lowest estimate of survival. For the bigeye thresher, this approach yielded negative values of r. Thus, the probability of survival at age was fixed to the maximum estimate.

312

Survivalg (year⫺1)

Reference

76

0.85–0.90 (0.77–0.91)

N2 (6.2; 2.9; 1–14)

70

0.78–0.89 (0.81–0.92)

16 (21)

N2 (37; 14.6; 4–75)

45

0.30–0.86 (0.60–0.91)

0.087

32 (42)

N3 (12.7; 3.0; 9–18)

75

0.35–0.92 (0.80–0.93)

Tri (12, 13, 14)

0.061

25 (31)

Tri1 (3.9; 2–5)

70

0.85–0.93 (0.83–0.91)

375 422

Tri (7, 8.5, 10) Tri (11, 12.8, 14)

0.085 0.092

16 (21) 20 (26)

–1 (2) –1 (2)

174 137

0.77–0.89 (0.85–0.90) 0.81–0.90 (0.82–0.91)

630

Tri (2, 3.5, 5)

0.158

15 (20)

Tri1 (4; 2–4)

136

0.35–0.83 (0.83–0.93)

Bonfil et al. (1993); Castro (1983) Seki et al. (1998); Lessa et al. (1999) Castro and Mejuto (1995); Pratt (1979); Skomal and Natanson (2003) Mollet et al. (2000); Natanson et al. (2006) Aasen (1963); Campana et al. (2002); Natanson et al. (2002) Liu et al. (1999) Chen et al. (1997); Liu et al. (1998) Cailliet et al. (1983)

Population

Maximum sizeb (cm TL)

Age at maturityc (years)

kd (year⫺1)

Life spane (years)

Fecundityf (pups per litter)

Carcharhinus falciformis

308

Tri (11, 12, 13)

0.091

22 (29)

N2 (10.2; 1.3; 6–14)

Carcharhinus longimanus

272

Tri (5, 6.5, 8)

0.099

17 (22)

Prionace glauca

327

Tri (4, 5, 6)

0.13

Isurus oxyrinchus

375

Tri (17, 18, 19)

Lamna nasus

360

Alopias pelagicus Alopias superciliosus Alopias vulpinus a

Offspring size (cm TL)

See text for information on the populations used for this analysis. TL is cm total length. c Values in parentheses are low, likeliest, and high from a triangular distribution (Tri). d k is the growth coefficient from the von Bertalanffy growth function. e Maximum empirical age; values in parentheses are ⫹30% of the first value. f Values in parentheses after the distribution name are mean, standard deviation, and range (normal distribution, N) or likeliest value and range (triangular distribution, Tri). All values extracted from these distributions were divided by two to account for an assumed 1:1 male-to-female embryo ratio and then by one, two, or three to account for the length of the reproductive cycle in years, which is indicated by a superscript after the distribution name. g Range of annual survivorship values obtained from six indirect life-history methods; values in parentheses show the range of age-specific estimates obtained through the weightbased method (see text for an explanation). b

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Table 27.1 Values of life-history traits used in a principal component analysis, and statistical distributions and values of demographic traits used in Monte Carlo simulation of population statistics for eight species of pelagic sharks.a

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Fecundity-at-age was generally represented by a normal distribution with the mean and standard deviation obtained or calculated from the literature and the reported range in litter size used to bound the distribution (Table 27.1). If the mode was reported instead of the mean, a triangular distribution was assumed with the range used to bound the distribution. A constant value of two pups per litter was assumed for the pelagic and bigeye threshers (Table 27.1). A 1:1 male-to-female ratio was assumed in all cases and also that 100% of females were reproductively active 1 year after reaching maturity. Annual reproductive cycles were assumed for the porbeagle and the three thresher species, a biennial cycle for the three carcharhinid species, and a triennial cycle for the shortfin mako. Annual fecundity was thus expressed as the number of female offspring at birth divided by the length of the reproductive cycle in years. Annual population growth rates (λ ⫽ er) were obtained from per capita rates of population increase (r) calculated through the discrete form of the Euler–Lotka equation as described in Cortés (2002). Generation time (here called T) was calculated as the mean age of mothers of newborn sharks when the population is in a stable age distribution (Caswell, 2001, p. 129). The reproductive value distribution (vx) and stable age distribution (cx) were also calculated as described in Cortés (2002). In matrix formulation, λ was calculated as the dominant eigenvalue of a Leslie matrix. The reproductive value (v) and stable age (w) distribution vectors were obtained as the left and right eigenvectors, respectively, associated with the dominant eigenvalue of the Leslie matrix. Elasticities (proportional sensitivities) of matrix elements (eij) were calculated as described in Caswell (2001). Elasticities for age-0 survival or fertility, juvenile survival, and adult survival were calculated by summation of matrix element elasticities across relevant age classes. The sum of all matrix element elasticities is 1. Formulas and more details are given in Cortés (2002).

The simulation and projection process A set of values for age-specific survival, age-specific fertility, age at first reproduction, and life span was randomly selected from the probability distribution describing each individual life-history trait. That set of variables was then used to construct a life table and an age-based matrix population model and elasticity matrix, from which the population statistics of interest (λ, T, and fertility, juvenile survival, and adult survival elasticities) were estimated at each iteration. Medians and frequency distributions for those parameter estimates were obtained after 10,000 iterations of the life table and population matrix model for each population analyzed. Confidence intervals for the population statistics were obtained as the 2.5th and 97.5th percentiles of each distribution. All simulations were implemented using Microsoft Excel spreadsheet software equipped with proprietary add-in risk assessment (Crystal Ball 2000, Decisioneering Inc., Denver, CO) and matrix function (MatriXL v. 4.5, MathTools Ltd., Ft. Washington, PA) software, and Microsoft Visual Basic. (Reference to trade names does not imply endorsement by the National Marine Fisheries Service, NOAA.) The position of the inflection point of population growth curves (R) was estimated by solving the linear equation derived by Fowler (1988) based on data for various animal species: R ⫽ 0.633 ⫺ 0.187(ln(rT))

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where rT is the dimensionless rate of increase per generation, calculated here using the median values of r and T obtained from Monte Carlo simulation.

Results Differences in life-history traits among pelagic shark species The PCA revealed that the first three components explained about 94% of the variance in life-history traits (Table 27.2). The first factor explained 45% of the variance in the five variables and correlated positively with adult body size, offspring size, and k, and negatively with longevity. The second and third factors explained 35% and 15% of the variance, respectively. The second factor mainly correlated positively with fecundity and k, and negatively with offspring size, whereas the third factor mainly correlated positively with longevity and adult body size. The second factor helps to isolate the pelagic and bigeye threshers because of low fecundity and large offspring size, and the blue shark for its high fecundity and small offspring. The first factor explains the positioning of the thresher shark by virtue of its large adult size and relatively fast growth completion rate (high k) and short life span. The shortfin mako/porbeagle and oceanic whitetip/silky shark are very close to each other because of their life-history similarities. The two lamnids share similar adult and offspring size, annual fecundity, low k, and relatively high longevity, whereas the two carcharhinids share similar characteristics (Fig. 27.1(a)). The third factor helps in separating the shortfin mako/porbeagle and silky/oceanic whitetip shark as a result of the higher longevity of the shortfin mako and silky shark, respectively. Cluster analysis confirmed the positioning of species in the plot of components 1 and 2 (Fig. 27.1(a)) by placing very closely the shortfin mako and porbeagle, the pelagic and bigeye threshers, and the oceanic whitetip and silky sharks, whereas the blue and thresher sharks were more separated from the rest (Fig. 27.1(b)).

Simulation of population parameters and elasticities, and position of the inflection point of population growth curves Population growth rates for the species of pelagic sharks analyzed varied widely, ranging from high values for the blue shark to values very close to zero for the shortfin mako and Table 27.2 Results of a PCA of five life-history traits for eight species of pelagic sharks.* Life-history trait

Component 1

Component 2

Component 3

Adult body length Annual fecundity Offspring length Growth coefficient (k) Longevity

0.56 ⫺0.06 0.45 0.51 ⫺0.47

⫺0.13 0.71 ⫺0.49 0.42 ⫺0.25

0.59 0.02 ⫺0.27 0.26 0.72

44.5

35.1

14.7

Percentage of total variance

* Values shown are the loadings (eigenvectors) of the first three components and the percentage of the total variance explained by each component.

Component 2

High fecundity Small offspring High k

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315

3 gla 2

1 Ion

vul

fal

0

Low fecundity Large offspring Low k

oxy ⫺1

nas

⫺2 ⫺2

sup

⫺1

pel

0

2

1

3

4

(a) Small size Low k High longevity Small offspring

Large size High k Low longevity Large offspring

Component 1

2.8

Euclidean distance

2.4 2 1.6 1.2 0.8 0.4 0

fal

lon

oxy

nas

sup

pel

vul

gla

Clusters (b)

Fig. 27.1 (a) Plot of the component scores of the first and second factors from a PCA of five life-history traits of eight species of pelagic sharks. (b) Dendrogram (Euclidean measure, single linkage method) from a hierarchical cluster analysis of the scores of the first three factors obtained in the PCA. The groupings show similarities in life-history traits among species. Species codes are: gla: Prionace glauca; oxy: Isurus oxyrinchus; vul: Alopias vulpinus; pel: A. pelagicus; sup: A. superciliosus; nas: Lamna nasus; fal: Carcharhinus falciformis; lon: C. longimanus.

pelagic and bigeye threshers (Table 27.3). Generation times ranged from about 7 years in the thresher shark to about 25 years in the shortfin mako. The values of λ obtained from simulation corresponded fairly well with the positioning of species in the PCA plot (Fig. 27.1(a)) in that those species with lower λ tended to be located toward the bottom of the

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Table 27.3 Population growth rates (λ), generation times (T), and elasticities (summed across relevant age classes) for eight species of pelagic sharks obtained from Monte Carlo simulation.* Population

λ (year⫺1)

T (years)

Elasticity Fertility

Prionace glauca Carcharhinus falciformis Lamna nasus Isurus oxyrinchus Carcharhinus longimanus Alopias pelagicus Alopias vulpinus Alopias superciliosus

Juvenile survival Adult survival

1.254 (1.151–1.373) 8.4 (7.2–9.7) 10.7 (9.3–12.1) 58.6 (52.7–63.7) 30.7 (25.6–36.8) 1.076 (1.057–1.091) 14.3 (13.7–15.3) 6.5 (6.1–6.8) 77.3 (74.9–79.4) 16.2 (13.8–18.9) 1.051 (1.039–1.064) 18.5 (17.5–19.8) 1.008 (0.978–1.028) 24.8 (23.5–26.3) 1.069 (1.029–1.119) 11.1 (9.4–13.0)

5.1 (4.8–5.4) 3.9 (3.6–4.1) 8.2 (7.5–9.7)

69.1 (67.1–71.2) 25.8 (23.6–27.9) 71.8 (68.0–75.0) 24.3 (21.1–28.1) 57.9 (53.0–64.2) 33.9 (29.5–40.6)

1.013 (0.995–1.034) 12.7 (11.6–14.3) 7.3 (6.5–7.9) 65.5 (62.3–68.0) 27.2 (25.1–30.1) 1.090 (0.986–1.206) 7.5 (5.9–9.4) 11.6 (9.6–14.5) 46.7 (39.0–53.1) 41.7 (36.1–48.0) 1.009 (0.990–1.028) 17.2 (15.9–18.6) 5.6 (5.1–5.9) 71.4 (66.6–76.8) 23.0 (17.7–27.9)

*

Values shown are medians with 95% confidence intervals.

PCA plot, which was mostly associated with low fecundity, large offspring size, and low k, whereas the species with the highest λ, the blue shark, was located at the top of the PCA plot, which was associated mostly with high fecundity and small offspring size. Species with intermediate values of λ, such as the two carcharhinids and the thresher shark, were located toward the middle of the PCA plot. Juvenile and adult survival elasticities were always higher than fertility (age-0 survival) elasticities, indicating that the juvenile and adult stages exert the greatest influence on λ. Median fertility elasticities ranged from 3.9% in the shortfin mako to 11.6% in the thresher shark; median juvenile survival elasticities ranged from 46.7% in the thresher shark to 77.3% in the silky shark; and median adult survival elasticities ranged from 16.2% in the silky shark to 41.7% in the thresher shark (Table 27.3). Juvenile survival elasticities were the highest in all species, and adult survival elasticity was of similar magnitude only for the thresher shark. The position of the inflection point of population growth curves (R) varied from about 0.5K in the blue shark to very near 1.0K in the shortfin mako and pelagic and bigeye threshers (Fig. 27.2). Values of R for the oceanic whitetip, silky, porbeagle, and thresher sharks were intermediate (0.63–0.71). Median population growth rates (λ) for the eight species were negatively correlated with R (R2 ⫽ 0.92, n ⫽ 8; Fig. 27.2).

Discussion Links between life-history traits and population statistics of pelagic sharks: conservation and management implications The eight species of sharks analyzed display different sets of life-history traits that are ultimately reflected in differing population statistics, dynamics, and resilience to exploitation. The blue shark’s early age at maturity and high litter size translate into high rates of

Comparative Life History and Demography of Pelagic Sharks

1.1

317

sup

1.0

pel

0.9

oxy

0.8 R

vul 0.7 nas 0.6

lon gla

fal

0.5 0.4 1.0

1.1

1.2

1.3

␭ Fig. 27.2 Position of the inflection point of population growth curves (R) in relation to the mean population growth rate (λ) obtained through Monte Carlo simulation for eight pelagic shark species (see Fig. 27.1 for species codes). The line illustrates a nonlinear regression fitted to the data.

increase for this species, despite its smaller offspring, which are likely to be subjected to higher mortality rates than those from the other species. The thresher shark, silky shark, oceanic whitetip shark, and porbeagle exhibit more moderate rates of increase. Of these four species, the thresher shark has dissimilar life-history traits, but the other three share offspring of similar size (70–76 cm total length, TL), similar annual fecundities (3–5 pups per year), slow growth completion rates (k ⫽ 0.06–0.10), and moderate life span (17–25 years). The shortfin mako and two of the Alopias species (pelagic and bigeye threshers) had very low population growth rates. These three species share large adult size (375–422 cm TL), low annual fecundity (2–4), and low k values (0.08–0.09). The species groupings obtained in the PCA, based on a collection of available life-history characteristics, thus provided a good initial indication of the population growth rates of these species and their likely response to exploitation. Although the life-history information has changed notably for some of the populations analyzed by Cortés (2000), that study also found similarities in the life-history traits of pelagic shark species in a PCA and cluster analysis of 41 populations of sharks. Population growth rates of pelagic shark species were more sensitive to survival of the juvenile and adult stages than to survival of age-0 individuals or fecundity. This is in agreement with the general elasticity patterns found by Cortés (2002) for sharks and with findings for other long-lived marine species (Heppell et al., 1999) and mammals (Heppell et al., 2000). From a conservation perspective, it suggests that management actions should focus on protection of juveniles and adults rather than age-0 individuals. From a management perspective, minimum size limits and protection of reproductive females could be the most effective measures, as they would enhance juvenile and adult survival directly and reproductive output indirectly. However, conservation and management efforts should not be guided exclusively by elasticity analysis, as it is still unclear how actions directed at one particular stage may affect the dynamics of other life stages (Heppell et al., 2000). Furthermore, the use of regression (Wisdom and Mills, 1997) or correlation analysis (Cortés, 2002) in

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tandem with stochastic elasticity analysis has been advocated as a way to get a more complete picture of the life stages and vital rates that exert the greatest effect on population growth rates and their variance.

Interpretation of rates of increase and the position of the inflection point of population growth curves In addition to portraying the demography of the eight species analyzed, one of the main objectives was to provide a relative scale for interspecific comparison by consistently applying the same assumptions to specify the statistical distributions describing demographic traits. The values of λ obtained should thus be regarded as relative indices rather than predictors of absolute population growth through time. Among the factors that may have affected results are the theoretical framework used, that is, the implicit model assumptions about density independence versus density dependence, and the demographic traits used. Life tables/matrix population models project observed vital rates into the future assuming density independence and time invariability, and predict that the population will grow exponentially at a rate r and reach a stable age distribution. In contrast, a traditional interpretation of fisheries models is that unexploited populations have reached carrying capacity (K) and are therefore at equilibrium (r ⫽ 0), thus allowing for positive growth rates only after a population or stock has been exploited and it recovers through logistic growth as a result of a compensatory, positive density-dependent response. Density dependence can also be incorporated into life tables or matrix population models either explicitly, by adding a term for density dependence in the model (Grant and Benton, 2000), or implicitly, by assuming that it is built into the vital rates used in the projection of population growth rates. In the present analysis, the latter approach was taken by using statistical distributions that favored higher values of survivorship at age to try to incorporate a potential compensatory densitydependent response to exploitation. The resulting population growth rates should thus be regarded as approximating the maximum biologically possible limit at low population densities. Regardless of whether these models incorporate density independence or density dependence, the lack of a time-dependent abundance vector in studies of shark populations implies that they do not capture the dynamics of the population, and should thus be viewed as static age-structured models. In using this type of model it is therefore important to consider when the vital rate information was collected relative to the duration and extent of harvesting of each population, because the onset and magnitude of potential compensatory densitydependent responses may vary accordingly (Smith et al., 1998). The eight populations analyzed are all exploited to different degrees, and it is possible that some of the vital rates used in the analyses may have changed as a result of density dependence and that the predicted population growth rates do not reflect what would be expected from projecting present vital rates. The rapidness and magnitude of a potential density-dependent response are also likely related to the life-history strategy and elasticity profile of each population. For a given level of exploitation, those populations with both low values of λ and high ratios of juvenile survival to fertility elasticity and adult survival to fertility elasticity (Cortés, 2002), such as the pelagic and bigeye threshers, probably

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take longer to show comparatively smaller compensatory changes than populations with high values of λ and low elasticity ratios, such as the blue shark. Using incorrect life-history traits can also obviously lead to inaccurate interpretations of population parameters. While only populations with published life-history information were included in the analysis, some of the demographic traits used may still have been incorrect. For example, age has only been validated through direct methods in the porbeagle (Natanson et al., 2002) and shortfin mako (Natanson et al., 2006). Data on age, growth, and sexual maturity of the thresher shark in the northeastern Pacific have just been revised (Smith et al., 2008b). Use of these revised data would likely have resulted in a more pessimistic assessment of the capacity of the thresher shark to withstand exploitation. Although the use of Monte Carlo simulation was intended to compensate in part for this problem by including a wide range of variation in the estimates of vital rates and statistical distributions thought to capture the biology of each population to minimize the occurrence of unrealistic combinations of vital rates, the type of distribution used and the range of variation in its values, and covariance among demographic traits, are other potential sources of variability that must be investigated. The population growth rates and generation times obtained with life tables/matrix population models for the eight species of pelagic sharks examined resulted in the prediction from Fowler’s regression equation that the populations would reach MSY at or well above 0.5K. This is consistent with predictions from Fowler (1988) and Restrepo et al. (1998), but there are views advocating that slow-growing fishes such as sharks would reach MSY at 0.30–0.40K (Thompson, 1992; Au et al., 2008) based on stock–recruitment considerations. One of the main implications resulting from reaching MSY at population sizes above 0.5K is that depleted stocks (low population sizes) will take longer to recover because the production curve is no longer parabolic, but instead is maximized at stock sizes ⬎0.5K. The findings obtained through Fowler’s regression equation must be interpreted cautiously. That equation may be biased because it was based on a limited number of species showing strong K- or r-selected tendencies for which estimates of both the rate of increase per generation and the position of the inflection point (fraction of carrying capacity, R) in population growth curves were available from the literature. However, the lack of information on R for shark populations precluded testing independently whether this parameter is correlated with population statistics such as λ or the rate of increase per generation. Despite its shortcomings, Fowler’s proposed equation is useful because it allows us to place the species compared along a gradient of R values. Ultimately, it has heuristic value, underscoring the need for further studies and analyses to gain insight into the poorly known population dynamics of sharks in general. There is mounting concern about the status of shark populations worldwide. While there is little doubt that many populations – especially those of pelagic species – have decreased substantially from their levels prior to the development of modern mechanized fishing fleets, the extent of the declines is the subject of intense debate (Baum et al., 2003, 2005; Baum and Myers, 2004; Burgess et al., 2005a, b). On the basis of our present knowledge of the biology of pelagic shark species, there is a gradient in the level of exploitation that different species can sustain. It is clear, however, that recovery time for most species whose stocks are heavily depleted will be long based on the position of the inflection point of their population growth curves as found in the present analysis.

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Acknowledgments I thank Merry Camhi, Ellen Pikitch, Beth Babcock, and the Ocean Wildlife Campaign for supporting my travel to the International Pelagic Shark Workshop and for organizing the publication of this volume. The views expressed in this chapter are those of the author and do not necessarily reflect the view of NOAA or any of its subagencies.

References Aasen, O. (1963) Length and growth of the porbeagle (Lamna nasus, Bonnaterre) in the Northwest Atlantic. Report on Norwegian Fishery and Marine Investigations 13, 20–37. Au, D. W., Smith, S. E. and Show, C. (2008) Shark productivity and reproductive protection, and a comparison with teleosts. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Baum, J. K. and Myers, R. A. (2004) Shifting baselines and the decline of pelagic sharks in the Gulf of Mexico. Ecology Letters 7, 1–11. Baum, J. K., Myers, R. A., Kehler, D. G., Worm, B., Harley, S. J. and Doherty, P. A. (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299, 389–392. Baum, J. K., Kehler, D. and Myers, R. A. (2005) Robust estimates of decline for pelagic shark populations in the Northwest Atlantic and Gulf of Mexico. Fisheries 30, 27–29. Benton, T. G. and Grant, A. (1999) Elasticity analysis as an important tool in evolutionary and population ecology. Trends in Ecology and Evolution 14, 467–471. Bonfil, R., Mena, R. and de Anda, D. (1993) Biological parameters of commercially exploited silky sharks, Carcharhinus falciformis, from the Campeche Bank, Mexico. In: Conservation Biology of Elasmobranchs (ed. S. Branstetter). NOAA Technical Report NMFS 115. NOAA/NMFS, Silver Spring, MD, pp. 73–86. Burgess, G. H., Beerkircher, L. R., Cailliet, G. M., Carlson, J. K., Cortés, E., Goldman, K. J., Grubbs, R. D., Musick, J. A., Musyl, M. K. and Simpfendorfer, C. A. (2005a) Is the collapse of shark populations in the Northwest Atlantic Ocean and Gulf of Mexico real? Fisheries 30, 19–26. Burgess, G. H., Beerkircher, L. R., Cailliet, G. M., Carlson, J. K., Cortés, E., Goldman, K. J., Grubbs, R. D., Musick, J. A., Musyl, M. K. and Simpfendorfer, C. A. (2005b) Reply to “Robust estimates of decline for pelagic shark populations in the Northwest Atlantic Ocean and Gulf of Mexico.” Fisheries 30, 30–31. Cailliet, G. M., Martin, L. K., Harvey, J. T., Kusher, D. and Weldon, B. A. (1983) Preliminary studies on the age and growth of the blue shark, Prionace glauca, common thresher, Alopias vulpinus, and shortfin mako, Isurus oxyrinchus, from California waters. In: Proceedings of the International Workshop on Age Determination of Oceanic Pelagic Fishes: Tunas, Billfishes, and Sharks (eds. E. D. Prince and L. M. Pulos). NOAA Technical Report NMFS 8. NOAA/NMFS, Silver Spring, MD, pp. 179–188. Campana, S. E., et al. (2002) Population dynamics of the porbeagle in the Northwest Atlantic Ocean. North American Journal of Fisheries Management 22, 106–121. Castro, J. A. and Mejuto, J. (1995) Reproductive parameters of blue shark, Prionace glauca, and other sharks in the Gulf of Guinea. Marine and Freshwater Research 46, 967–973. Castro, J. I. (1983) The Sharks of North American Waters, 1st edn. Texas A&M University Press, College Station, TX. Caswell, H. (2001) Matrix Population Models: Construction, Analysis, and Interpretation, 2nd edn. Sinauer Associates, Sunderland, MA.

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Chen, C. T., Liu, K. M. and Chang Y. C. (1997) Reproductive biology of the bigeye thresher shark, Alopias superciliosus (Lowe, 1839) (Chondrichthyes: Alopiidae), in the northwestern Pacific. Ichthyological Research 44, 227–235. Cortés, E. (1999) A stochastic stage-based population model of the sandbar shark in the western North Atlantic. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 115–136. Cortés, E. (2000) Life history patterns and correlations in sharks. Reviews in Fisheries Science 8, 299–344. Cortés, E. (2002) Incorporating uncertainty into demographic modeling: Application to shark populations and their conservation. Conservation Biology 16, 1048–1062. De Kroon, H., Plaisier, A., van Groenendael, J. and Caswell, H. (1986) Elasticity: The relative contribution of demographic parameters to population growth rate. Ecology 67, 1427–1431. Ebert, T. A. (1999) Plant and Animal Populations: Methods in Demography. Academic Press, San Diego, CA. Fowler, C. W. (1981a) Density dependence as related to life history strategy. Ecology 62, 602–610. Fowler, C. W. (1981b) Comparative population dynamics in large mammals. In: Dynamics of Large Mammal Populations (eds. C. W. Fowler and T. Smith). John Wiley & Sons, New York, pp. 437–455. Fowler, C. W. (1987) A review of density dependence in populations of large mammals. In: Current Mammalogy (ed. H. Genoways). Plenum Press, New York, pp. 401–441. Fowler, C. W. (1988) Population dynamics as related to rate of increase per generation. Evolutionary Ecology 2, 197–204. Grant, A. and Benton, T. G. (2000) Elasticity analysis for density-dependent populations in stochastic environments. Ecology 81, 680–693. Heppell, S. S., Crowder, L. B. and Menzel, T. R. (1999) Life table analysis of long-lived marine species, with implications for conservation and management. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 137–148. Heppell, S. S., Caswell, H. and Crowder, L. B. (2000) Life histories and elasticity patterns: Perturbation analysis for species with minimal demographic data. Ecology 81, 654–665. Lessa, R., Marcante Santana, F. and Paglerani, R. (1999) Age, growth and stock structure of the oceanic whitetip shark, Carcharhinus longimanus, from the southwestern equatorial Atlantic. Fisheries Research 42, 21–30. Liu, K. M., Chiang, P. J. and Chen, C. T. (1998) Age and growth estimates of the bigeye thresher shark, Alopias superciliosus, in northeastern Taiwan waters. Fishery Bulletin 96, 482–491. Liu, K. M., Chen, C. T., Liao, T. H. and Joung, S. J. (1999) Age, growth, and reproduction of the pelagic thresher shark, Alopias pelagicus, in the northwestern Pacific. Copeia 1999, 68–74. Mollet, H. F. and Cailliet, G. M. (2002) Comparative population demography of elasmobranchs using life history tables, Leslie matrices and stage-based matrix models. Marine and Freshwater Research 53, 503–516. Mollet, H. F., Cliff, G., Pratt, H. L. and Stevens, J. D. (2000) Reproductive biology of the female shortfin mako, Isurus oxyrinchus Rafinesque, 1810, with comments on the embryonic development of lamnoids. Fishery Bulletin 98, 299–318. Natanson, L. J., Mello, J. J. and Campana, S. E. (2002) Validated age and growth of the porbeagle shark (Lamna nasus) in the western North Atlantic Ocean. Fishery Bulletin 100, 266–278. Natanson, L. J., Kohler, N. E., Ardizzone, D., Cailliet, G. M., Wintner, S. P. and Mollet, H. F. (2006) Validated age and growth estimates for the shortfin mako, Isurus oxyrinchus, in the North Atlantic Ocean. Environmental Biology of Fishes 77, 367–383. Pratt, H. L. (1979) Reproduction in the blue shark, Prionace glauca. Fishery Bulletin 77, 445–457.

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Restrepo, V. R., et al. (1998) Technical Guidance on the Use of Precautionary Approaches to Implementing National Standard 1 of the Magnuson-Stevens Fishery Conservation and Management Act. NOAA Technical Memorandum NMFS-F/S. NOAA/NMFS, Silver Spring, MD, 54 pp. Seki, T., Taniuchi, T., Nakano, H. and Shimizu, M. (1998) Age, growth and reproduction of the oceanic whitetip shark from the Pacific Ocean. Fisheries Science 64, 14–20. Skomal, G. B. and Natanson, L. J. (2003) Age and growth of the blue shark, Prionace glauca, in the North Atlantic Ocean. Fishery Bulletin 101, 627–639. Smith, S. E., Au, D. W. and Show, C. (1998) Intrinsic rebound potentials of 26 species of Pacific sharks. Marine and Freshwater Research 49, 663–678. Smith, S. E., Au, D. W. and Show, C. (2008a) Intrinsic rates of increase in pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Smith, S. E., Rasmussen, R. C., Ramon, D. A. and Cailliet, G. M. (2008b) The biology and ecology of thresher sharks (Alopiidae). In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Thompson, G. G. (1992) Management advice from a simple dynamic pool model. Fishery Bulletin 90, 552–560. Wisdom, M. J. and Mills, L. S. (1997) Sensitivity analysis to guide population recovery: Prairiechickens as an example. Journal of Wildlife Management 61, 302–312. Wisdom, M. J., Mills, L. S. and Doak, D. F. (2000) Life stage simulation analysis: Estimating vitalrate effects on population growth for conservation. Ecology 81, 628–641.

Chapter 28

Molecular Markers and Genetic Population Structure of Pelagic Sharks Edward J. Heist

Abstract Understanding the genetic population structure of pelagic sharks is crucial for the management and conservation of these widespread but vulnerable fishes. Despite their great potential for migration and movement, isolated stocks of pelagic sharks may exist within and between ocean basins. Sharks exhibit several characteristics (e.g., wide distributions, long generation times, extensive movement) that make the detection of genetic stock structure a challenge. Overcoming these difficulties requires international collaborations and sampling protocols that can be performed at sea without specialized laboratory equipment. While a variety of molecular markers are available for studying pelagic sharks, the marker should be chosen carefully to provide an appropriate level of resolution to maximize power in statistical analyses. Genetic studies are complementary rather than redundant to traditional tag/recapture studies. Because a small amount of migration can homogenize allele frequencies among stocks, significant differences in allele frequencies among regions indicate that multiple independent stocks are present, while nonsignificant differences cannot refute the presence of separate fishery stocks. Key words: conservation genetics, fishery stocks, fishery management, genetics, population genetics, molecular markers.

Introduction Pelagic sharks present fishery managers and conservation biologists with unusual challenges. Because these sharks are distributed across vast stretches of open ocean, it is extremely difficult to estimate population sizes and delineate stocks. Many species migrate across national borders or into international waters, where they may be exploited by fishers of several nations (Kohler et al., 1998; Musick et al., 2000). A better understanding of the distribution and number of discrete stocks of these abundant but vulnerable fishes is crucial to their conservation and management. Analysis of polymorphic genetic markers is one way to identify distinct fishery stocks (reviewed in Carvalho and Hauser, 1994; Ward and Grewe, 1994) and to forensically identify sharks and shark parts to species (Shivji et al., 2008). Populations that are reproductively Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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isolated acquire different frequencies of polymorphic (multi-allelic) genes through genetic drift and perhaps natural selection. The rate of genetic drift is inversely proportional to the effective size (Ne) of the population, therefore the allele frequencies of small populations drift at a faster rate than those of large populations. Migration (m) counteracts genetic drift, and so populations that routinely exchange breeding individuals will maintain similar allele frequencies. If sufficient time has passed since the establishment of a pattern of gene flow (migration) and genetic drift, a constant variance in allele frequencies among stocks will be maintained. The standardized variance in allele frequencies (FST) can be calculated using frequencies of polymorphic characters among geographic locations. The equilibrium relationship between FST and Nem is FST
1/(4Nem  1) for nuclear genes and FST
1/(2Nemf  1) for mitochondrial genes. The term Nemf in the second equation refers to the effective number of female migrants per generation. These relationships are based on the island model of migration (Wright, 1969). Although this model is biologically unrealistic for pelagic sharks, other patterns of migration are believed to produce a similar relationship between Nem and FST (Crow and Aoki, 1984). One caveat to this analytic approach is that the relationship between Nem and FST assumes equilibrium between migration and drift. If two populations have been isolated only recently, the value of FST will indicate a larger amount of migration than is currently occurring. The number of generations required to reach migration/drift equilibrium may number in the hundreds of thousands in cases where the migration rate is small (Waples, 1998) and/or the effective population size is large. Some pelagic sharks have long generation lengths and will therefore approach equilibrium at a slower rate than species with shorter generation lengths. However, high rates of migration among pelagic shark populations allow an approach to equilibrium in fewer generations than for species with more disjunct populations. A more serious difficulty in applying this model to pelagic sharks is that, given their high migration potential, FST values are expected to be very low. Marine species tend to have lower FST values than freshwater or anadromous species (Ward et al., 1994), and pelagic marine species have especially low FST values owing to their great potential for dispersal. When testing for the presence of multiple genetic stocks, the appropriate null hypothesis is that all samples come from a single genetic stock and therefore FST
0. Rejection of the null hypothesis indicates the presence of two or more genetic stocks. The closer the true value of FST is to zero, the greater the statistical power that is necessary to reject the null hypothesis. When FST values are low, a small error associated with the measurement of FST can produce a large difference in estimates of Nem. Fortunately, the number of migrants per generation need not be estimated with great precision because the amount of migration (gene flow) that reduces the magnitude of FST to barely detectable levels is usually much lower than the level of migration necessary to replenish overexploited stocks (see below). While this may not be the case for species with high fecundities in which migrational recruitment from a small number of adults can produce a large number of offspring, the low fecundities of many pelagic sharks reduce the potential impact of migration on stock recovery. Failure to detect a small but nonzero FST (a type II error) may lead to the erroneous conclusion that a single fishery stock exists. The results of a type II error may be more detrimental to sustained management than the spurious rejection of a hypothesis that FST
0 (type I error). One obvious remedy to this problem is to increase sample sizes (numbers of individuals per sample) to increase statistical power. Other remedies include

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lowering the α-level (i.e., below the traditional criterion of p  0.05 used to reject null hypotheses) to reduce the likelihood of a type II error (Dizon et al., 1995) and examining tag/recapture data (Ryman et al., 1995; Waples, 1998). While traditional tag/recapture studies are also very useful for identifying unique stocks of pelagic sharks (Kohler et al., 1998; Kohler and Turner, 2008), tagging and genetics methodologies provide complementary but not identical information. Results of tag/recapture studies provide direct data on the gross movements of individuals, often indicating that some sharks move great distances. However, not all sharks that move are “effective migrants” in the context of stock dynamics and population genetics. If a shark dies or returns to its natal population prior to reproduction, it may have “moved” but it has not “migrated” in the sense that it will not have contributed to recruitment of the nonnative stock. The use of multiple highly polymorphic loci and the ability to rapidly screen large numbers of individuals have greatly increased the power of resolving small but significant differences in allele frequencies among fish populations. In a large study of mitochondrial DNA from 1,675 red drum (Sciaenops ocellatus), Gold et al. (1999) detected a statistically significant FST value of 0.002, indicating an equilibrium migration of 250 females per generation among sample locations. The robust statistical power of such data-rich studies has led to considerable discussion regarding the distinction between the “statistical” and “biological” significance of small differences in allele frequencies among samples (Waples, 1998; Hedrick, 1999). Small differences in the frequencies of neutral genetic markers indicate that there is some degree of reproductive isolation among stocks, and thus even if there are no adaptive differences, the stock structure may be “biologically significant” in the sense that it indicates barriers to migrational recruitment. While much of the literature on the harmful effects of human-mediated stock transfer in fishes involves species that are readily transported or captive-reared, pelagic sharks are notoriously difficult to breed, transport, or maintain in captivity. Intentional mixing of sharks for restoring overexploited stocks (as is routinely done with coastal and freshwater fisheries) is impractical, and so recruitment of an overexploited shark stock must come from natural reproduction within the geographic boundaries of the original stock. Thus small but significant differences in allele frequencies are almost certainly “biologically significant” in pelagic sharks because they indicate a restriction in migration among regions that cannot be circumvented by manipulative means (e.g., hatcheries, transport). Even with the enhanced power offered by multiple polymorphic microsatellite loci, a significant FST value almost always indicates that migrational recruitment will be an ineffectual force in the replenishing of an exploited stock. Waples (1998) cautions that the smaller the genetic “signal” the greater the likelihood that “noise” will lead to a false rejection (type I error) of the null hypothesis, and therefore great care must be taken to avoid systematic errors. For example, individuals from different samples should be run on the same gel to avoid a sample-specific bias in scoring allele sizes.

Molecular markers Molecular markers can be categorized into protein-based markers (e.g., allozymes) and DNAbased markers. The latter can be further divided into mitochondrial and nuclear markers.

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Each type of molecular marker has distinct strengths and weaknesses (cost, required tissue quality, resolution) regarding its proven and potential utility for studies in pelagic sharks. Allozyme electrophoresis was the first method widely used to assess the genetic structure of marine fish populations (Utter, 1991). Allozymes are different allelic forms of (usually) enzymatic proteins. To detect allozyme variation, tissue samples are homogenized in a grinding buffer to release water-soluble proteins into solution. The solution is then applied to a separatory medium (usually starch or cellulose acetate) and subjected to an electric field in which proteins migrate differentially according to their charge, size, and three-dimensional shape. Zones of enzymatic activity are identified by staining the gel (or plate) with a mixture that includes enzymatic substrates, cofactors, and an indicator dye (Murphy et al., 1996). Each individual is scored as either heterozygous or homozygous for a particular gene locus. Allele frequencies are tabulated within samples, and differences in allele frequencies among samples are used to estimate FST. Allozymes are relatively inexpensive to score and require less specialized equipment than DNA-based methods (Murphy et al., 1996). However, allozymes have several serious drawbacks for use in pelagic sharks. One weakness is that sharks typically exhibit low levels of protein polymorphism, which reduces the power to discriminate stocks. In a study of 20 blue sharks (Prionace glauca, Carcharhinidae), Smith (1986) noted that only 3 of 27 loci were polymorphic (mean heterozygosity
0.037). Eitner (1995) found only one heterozygote in six shortfin mako sharks (Isurus oxyrinchus, Lamnidae) screened with 14 presumptive allozyme loci. Allozyme variation within the three recognized species of thresher sharks (Alopias vulpinus, A. superciliosus, and A. pelagicus, Alopiidae) was similarly low, but one sample of thresher sharks was homozygous for alternate alleles at several loci, suggesting the presence of an unrecognized species (Eitner, 1995). Another disadvantage of allozymes is that freshly collected tissues from multiple organs are typically necessary to score a representative number of loci, thus nonlethal and dockside sampling for allozyme analysis is impractical. Shipboard sampling requires liquid nitrogen, dry ice, or ultracold freezers, all of which present logistical challenges on research or fishing vessels. The lack of genetic variation and the difficulty of collecting adequate tissue samples make it unlikely that allozymes will be the method of choice for genetic studies of pelagic sharks, especially as DNA-based technologies become cheaper and more widely available. DNA in animal cells is present in two organelles: the nuclei and the mitochondria. The vast majority of DNA is located in nuclei, where two copies (one from each parent) of most functional gene loci are found. The mitochondria possess a single small loop of maternally inherited DNA (mtDNA) that in vertebrates is approximately 1.7  104 basepairs in length. In contrast, the diploid nuclear genome of the shortfin mako is approximately 8  109 base-pairs in length (E. J. Heist, unpublished data). The mitochondrial genome of vertebrates consists of 14 protein-coding genes and two ribosomal RNA (rRNA) genes alternating with 22 short transfer RNA (tRNA) genes (Meyer, 1993). A single noncoding region (the D-loop or control region) contains regulatory elements and the replication origin of one of the mtDNA strands. Most intraspecific variation is in the form of “silent” substitutions in the third codon position of the proteincoding genes or substitutions or insertions/deletions (indels) variation in the D-loop region. In terms of single-base substitutions, mtDNA evolves approximately 10 times faster than nuclear DNA (Brown et al., 1979), resulting in high levels of intraspecific

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variation, although mtDNA evolves more slowly in sharks than in mammals (Martin et al., 1992). Because mtDNA is haploid and maternally inherited, it has an approximately fourfold lower effective population size than nuclear genes and therefore undergoes genetic drift at a faster rate than nuclear genes (Wilson et al., 1985). This accelerated rate results in higher FST values and greater power for detecting stock structure; however, mtDNA-derived FST values indicate only movements of females since (presumably) male sharks do not contribute mtDNA to their offspring. If sufficient fresh or frozen material is present, intact mtDNA can be purified from nuclear DNA using cesium chloride ultracentrifugation (Sambrook and Russell, 2001). By subjecting this compact molecule to restriction enzymes, which cleave double-stranded DNA at specific four- or six-base motifs, a small number of fragments are produced. These fragments can be labeled with either a radioactive label or a chemiluminescent tag, separated on agarose or polyacrylamide gels, and visualized via autoradiography or the use of an imaging system. A much smaller concentration of mtDNA fragments, perhaps with significant nuclear DNA contamination, can be visualized by first transferring the separated fragments to a solid support (Southern transfer) and probing with purified and labeled mtDNA from a related species (Sambrook and Russell, 2001). Variations in the fragment patterns produced in different individuals are scored as a subset of the differences in the DNA sequences of the individuals. Estimates of the mean genetic difference among individuals are used to compute various estimators of FST, which can be thought of as the among-sample component of genetic variation. Mitochondrial DNA variation can also be scored using the polymerase chain reaction (PCR) to amplify specific regions followed by direct sequencing or restriction digestion. PCR technology allows the generation of data from minute pieces of tissue (e.g., fin clips) and thus allows for nonlethal or dockside sampling. Amplification of specific regions of mtDNA followed by restriction fragment-length polymorphism (RFLP) or direct sequencing can reveal variation comparable to that determined from whole-molecule mtDNA RFLP, and does not require the high tissue quality and quantity needed for the latter method (Bernatchez and Danzmann, 1993). Nuclear DNA has several advantages over mitochondrial DNA. Because nuclear DNA is inherited equally from both parents, paternal as well as maternal gene flow can be assayed. While mtDNA consists of a single locus providing only one estimate of FST, nuclear markers can provide multiple independent estimates of FST and therefore the stochastic variation among estimates can be determined (Waples, 1998). Unlike mtDNA, nuclear DNA can also provide direct information about hybridization and paternity. While protein-coding nuclear genes have a very slow mutation rate, leading to low levels of intraspecific diversity, some nuclear DNA-based markers exhibit considerable variation. These markers include sequences of protein-coding gene introns and ribosomal DNA spacers (Palumbi and Baker, 1994), amplified fragment-length polymorphisms (Vos et al., 1995), major histocompatibility genes (Edwards and Potts, 1996), randomly amplified polymorphic DNA (Grossberg et al., 1996), anonymous single-copy nuclear genes (Karl, 1996), and variable-number tandem repeats (VNTRs) (Ashley and Dow, 1994). VNTR loci are a class of nuclear loci that possess a core motif that is repeated a variable number of times; the number of repeats (and hence the size of the amplified locus) is the source of genetic variation. VNTR core motifs range from one to six bases in length

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(microsatellites) or from six to several hundred bases (minisatellites). Among the different classes of nuclear loci, microsatellites have the greatest utility in conservation genetics and will likely prove the most useful nuclear markers for genetic studies of pelagic sharks in the near future. Microsatellites have a very high mutation rate and hence display a great deal of allelic diversity within populations (Ashley and Dow, 1994). The nonrepetitive flanking regions on either side of the core sequence are used to design PCR primers that will allow the microsatellite alleles to be readily amplified from genomic DNA. Examples of microsatellite repeat motifs include (GT)n and (GA)n, where the subscript refers to a variable number of times the core motif is repeated. When the number of uninterrupted repeats exceeds 10, the loci are typically very polymorphic (Weber, 1990). Some loci have 20 or more alleles within a single population and heterozygosities approaching unity (O’Connell and Wright, 1997). This extremely high allelic diversity makes microsatellites useful for paternity analyses because it is unlikely that maternal and paternal parents will share alleles. Thus, once the maternal alleles are assigned to each pup in a litter, the presence of more than two paternal alleles indicates that a clutch has multiple sires. Because the genomes of all vertebrates contain thousands of microsatellite loci, the power of the analysis is limited only by the number of loci the researcher chooses to develop. Although microsatellite loci have historically been difficult and expensive to develop, many loci can be amplified and scored in congeners or even closely allied genera, increasing their utility. For example, all five microsatellite loci developed in shortfin mako by Schrey and Heist (2002) are polymorphic in the lamnid species longfin mako (Isurus paucus), porbeagle (Lamna nasus), and salmon shark (L. ditropis), while two were polymorphic in white shark (Carcharodon carcharias, Lamnidae) and common thresher (A. vulpinus). Five of 16 microsatellite loci developed in the blacktip shark (Carcharhinus limbatus, Carcharhinidae) by Keeney and Heist (2003) were polymorphic in the pelagic blue shark. Once the loci are developed, it is possible for one person to score dozens of individuals for several loci in 1 day. Because microsatellites are scored using the PCR, data can be obtained from very small pieces of tissue (e.g., blood, biopsies, or fin clips), making nonlethal sampling possible.

Genetic stock structure of pelagic sharks The shortfin mako is the only species of pelagic shark for which sufficient data have been published to assess its stock structure. Heist et al. (1996) examined mtDNA RFLP patterns in 120 shortfin mako collected from the North Atlantic (New England and Flemish Cap), South Atlantic (Brazil), South Pacific (New South Wales), and North Pacific (southern California). That study detected significant heterogeneity in mtDNA haplotype frequencies between the North Atlantic sample and each of the other three samples. Furthermore, the North Atlantic sample exhibited significantly lower haplotype diversity than the other samples, indicating a smaller long-term effective population size, perhaps due to a historic bottleneck. Haplotypes that were present at high frequencies were detected in all samples, and there did not appear to be a phylogeographic pattern (e.g., location-specific lineages) indicative of complete isolation of stocks. Subsequent to this work, Schrey and Heist (2003) examined nuclear microsatellite loci in a larger number of shortfin mako specimens, including additional ones from the previously sampled locations and new ones from South

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Africa, and concluded that very small but statistically significant allele frequency differences occurred between locations. The small magnitudes of the FST values indicated the presence of some genetic exchange among sample locations. Thus both studies concluded that shortfin makos most likely comprise multiple fishery stocks with sufficient genetic exchange among the stocks to consider the shortfin mako a single worldwide species. Little is known about the locations and timing of mating and parturition in pelagic sharks. However, recent evidence summarized in Hueter et al. (2004) indicates that many if not most species of coastal sharks exhibit some degree of natal philopatry. Tagging data indicate that blacknose (Carcharhinus acronotus, Carcharhinidae) and blacktip sharks tagged in summer habitats, from which they are absent in winter months, return to the same locations in subsequent summers. Nurse (Ginglymostoma cirratum, Ginglymostomatidae) (Pratt and Carrier, 2001) and lemon (Negaprion brevirostris, Carcharhinidae) (Feldheim et al., 2002) shark females have been shown to faithfully return to the same pupping areas in alternate years. Pardini et al. (2001) inferred the presence of female natal philopatry based on much larger levels of genetic divergence in maternally inherited mtDNA markers than in biparentally inherited nuclear markers in white sharks. Members of discrete genetic stocks may exhibit considerable geographic overlap, and tagging data may even indicate movement among genetically distinct stocks. A genetic study that is keyed to specific life stages (e.g., neonates near parturition localities) may detect multiple genetic stocks in the presence of adult movement throughout a region as demonstrated by tag/recapture data. For example, Keeney et al. (2004) detected very high levels of heterogeneity in mtDNA haplotype frequencies among blacktip sharks from continental nursery areas in a study that employed only neonate and young-of-the-year sharks collected in close proximity to natal nurseries. Subsequent analyses of additional specimens using both mtDNA and nuclear microsatellite loci confirm that blacktip nurseries from the northwestern Atlantic, Gulf of Mexico, and Caribbean Sea exhibit very different mtDNA haplotype frequencies, while nuclear DNA allele frequencies are much more similar (Keeney et al., 2005). Thus, while little is known about the locations and extent of pelagic shark mating and nursery areas, insights from the more numerous studies of coastal sharks indicate that locating these areas in time and space will be critical to understanding the recruitment and stock structure of pelagic sharks. Future studies of genetic stock structure in pelagic sharks would benefit from attempts to sample adults or young sharks in or near nursery areas.

Conclusions Modern methods of gene frequency analysis provide a useful but limited means of identifying separate fishery stocks in pelagic sharks. Because of the high potential for gene flow in pelagic sharks, the magnitude of the variance in allele frequencies among stocks will be very small. Nevertheless, if the frequency differences are real (i.e., they are not due to methodological errors), they are likely to be genetically significant in terms of the effect of local exploitation on pelagic shark stocks. Because pelagic sharks lack any planktonic life stages, gene flow and migration occur only through the active movement of individuals. Since each species has unique reproductive and migrational tendencies, it is unlikely that any general patterns of gene flow or stock structure apply to all pelagic

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sharks. Discrete stocks may exist even in the presence of the movement of individuals among stocks as indicated by tag/recapture studies. Bowen (1999) opined that conservation geneticists fall into three camps, each with their own viewpoints and priorities. Systematists seek to preserve unique genetic lineages; ecologists seek to retain ecosystem function through the conservation of keystone species; and evolutionary biologists seek to preserve the future potential for adaptive evolution. The conservation of pelagic sharks is not likely to be a high priority for either the “systematist” or “evolutionary biologist” viewpoint because the widespread distribution of pelagic sharks makes it unlikely that any species will go extinct because of overfishing or habitat alteration on anything but a global scale. Even if an entire population was extirpated, the possibly high levels of gene flow and therefore lack of genetic divergence among populations make it unlikely that any unique adaptations would be lost from the species. Thus, it is only at the ecological level that pelagic shark conservation becomes important. Because it is impractical (if not impossible) to increase pelagic shark populations through any means other than natural reproduction and migration, a fuller understanding of demographics, stock structure, and migration rates among stocks is crucial. Though uncertainties remain regarding the importance of the role that sharks play as apex predators in marine ecosystems, it is clear that their life-history strategies make them much more vulnerable to overfishing than predatory teleosts, and that declines in pelagic shark populations may cause undesirable shifts in pelagic food webs (Schindler et al., 2002). The identification and conservation of regional shark stocks, without regard to adaptive differences or evolutionary novelty, are critical. Recent evidence suggests that in the North Atlantic, stocks of some pelagic sharks have been reduced to less than 20% of their pre-exploitation population levels (Baum et al., 2003). The authors of this report suggested that “carefully designed marine reserves in concert with reductions in fishing effort could hold promise for safeguarding sharks and other large predators from further declines and ecological extinction.” If such management practices are to be successful, they will need to be based on an understanding of the genetic stock structure of the species involved.

Acknowledgments The research on shortfin mako and blacktip sharks cited in this work was supported by the Southern Illinois University Office of Research and Development and by the National Science Foundation, respectively. The National Audubon Society’s Living Oceans Program supported my attendance at the pelagic shark conference and made this manuscript possible. I thank D. Keeney, A. Schrey, M. Shivji, and an anonymous reviewer for valuable comments on this manuscript.

References Ashley, M. V. and Dow, B. D. (1994) The use of microsatellite analysis in population biology: Background, methods and potential applications. In: Molecular Ecology and Evolution: Approaches and Applications (eds. B. Schierwater, B. Streit and R. DeSalle). Birkhauser Verlag, Basel, Switzerland, pp. 185–201.

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Baum, J. K., Myers, R. A., Kehler, D. G., Worm, B., Harley, S. J. and Doherty, P. A. (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299, 389–392. Bernatchez, L. and Danzmann, R. G. (1993) Congruence in control-region sequence and restriction site variation in mitochondrial DNA of brook charr (Salvelinus fontinalis Mitchill). Molecular Biology and Evolution 10, 1002–1014. Bowen, B. W. (1999) Preserving genes, species, or ecosystems? Healing the fractured foundations of conservation policy. Molecular Ecology 8, S5–S10. Brown, W. M., George, M. and Wilson, A. C. (1979) Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences 76, 1967–1971. Carvalho, G. R. and Hauser, L. (1994) Molecular genetics and the stock concept in fisheries. Reviews in Fish Biology and Fisheries 4, 326–350. Crow, J. F. and Aoki, K. (1984) Group selection for a polygenic behavioral trait: Estimating the degree of population subdivision. Proceedings of the National Academy of Sciences 81, 6073–6077. Dizon, A. E., Taylor, B. L. and O’Corry-Crowe, G. M. (1995) Why statistical power is necessary to link analyses of molecular variation to decisions about population structure. In: Evolution and the Aquatic Ecosystem (eds. J. L. Neilson and D. A. Powers). American Fisheries Society, Bethesda, MD, pp. 288–294. Edwards, S. V. and Potts, W. K. (1996) Polymorphism of genes in the major histocompatibility complex (MHC): Implications for conservation of vertebrates. In: Molecular Genetic Approaches in Conservation (eds. T. B. Smith and R. K. Wayne). Oxford University Press, New York, pp. 214–237. Eitner, B. J. (1995) Systematics of the genus Alopias (Lamniformes: Alopiidae) with evidence for the existence of an unrecognized species. Copeia 1995, 562–571. Feldheim, K. A., Gruber, S. H. and Ashley, M. V. (2002) The breeding biology of lemon sharks at a tropical nursery lagoon. Proceedings of the Royal Society of London, Series B 269, 1655–1661. Gold, J. R., Richardson, L. R. and Turner, T. F. (1999) Temporal stability and spatial divergence of mitochondrial DNA haplotype frequencies in red drum (Sciaenops ocellatus) from coastal regions of the western Atlantic Ocean and Gulf of Mexico. Marine Biology 133, 593–602. Grossberg, R. D., Levitan, D. R. and Cameron, B. B. (1996) Characterization of genetic structure and genealogies using RAPD-PCR markers: A random primer for the novice and nervous. In: Molecular Zoology: Advances, Strategies, and Protocols (eds. J. D. Ferraris and S. R. Palumbi). John Wiley & Sons, New York, pp. 67–100. Hedrick, P. W. (1999) Perspective: Highly variable loci and their interpretation in evolution and conservation. Evolution 53, 313–318. Heist, E. J., Musick, J. A. and Graves, J. E. (1996) Genetic population structure of the shortfin mako (Isurus oxyrinchus) inferred from restriction fragment length polymorphism analysis of mitochondrial DNA. Canadian Journal of Fisheries and Aquatic Sciences 53, 583–588. Hueter, R. E., Heupel, M. R., Heist, E. J. and Keeney, D. B. (2004) The implications of philopatry in sharks for the management of shark fisheries. Journal of Northwest Atlantic Fishery Science 35 (article 7). Karl, S. A. (1996) Application of anonymous nuclear loci to conservation biology. In: Molecular Genetic Approaches in Conservation (eds. T. B. Smith and R. K. Wayne). Oxford University Press, New York, pp. 38–83. Keeney, D. B. and Heist, E. J. (2003) Characterization of microsatellite loci isolated from the blacktip shark and their utility in requiem and hammerhead sharks. Molecular Ecology Notes 3, 501–504. Keeney, D. B., Heupel, M. R., Hueter, R. E. and Heist, E. J. (2004) Genetic heterogeneity among blacktip shark, Carcharhinus limbatus, continental nurseries along the US Atlantic and Gulf of Mexico. Marine Biology 3, 1039–1046.

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Keeney, D. B., Heupel, M. R., Hueter, R. E. and Heist, E. J. (2005) The genetic structure of blacktip shark (Carcharhinus limbatus) nurseries in the western Atlantic, Gulf of Mexico, and Caribbean Sea inferred from control region sequences and microsatellites. Molecular Ecology 14, 1911–1923. Kohler, N. E. and Turner, P. A. (2008) Stock structure of the blue shark (Prionace glauca) in the North Atlantic Ocean based on tagging data. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Kohler, N. E., Casey, J. G. and Turner, P. A. (1998) NMFS Cooperative Shark Tagging Program 1962–93: An atlas of shark tag and recapture data. Marine Fisheries Review 60, 1–87. Martin, A. P., Naylor, G. J. P. and Palumbi, S. R. (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357, 153–155. Meyer, A. (1993) Evolution of mitochondrial DNA in fishes. In: Biochemistry and Molecular Biology of Fishes (eds. P. W. Hochachka and T. P. Mommsen). Elsevier, New York, pp. 1–38. Murphy, R. W., Sites, J. M. J., Buth, D. G. and Haufler, C. H. (1996) Proteins: Isozyme electrophoresis. In: Molecular Systematics (eds. D. M. Hillis, C. Moritz and B. K. Mable). Sinauer Associates, Sunderland, MA, pp. 51–120. Musick, J. A., Burgess, G., Cailliet, G., Camhi, M. and Fordham, S. (2000) Management of sharks and their relatives (Elasmobranchii). Fisheries 25, 9–13. O’Connell, M. and Wright, J. M. (1997) Microsatellite DNA in fishes. Reviews in Fish Biology and Fisheries 7, 331–363. Palumbi, S. R. and Baker, C. S. (1994) Contrasting population structure from nuclear intron sequences and mtDNA of humpback whales. Molecular Biology and Evolution 11, 426–435. Pardini, A. T., Jones, C. S., Noble, L. R., Kreiser, B., Malcolm, H., Bruce, B. D., Stevens, J. D., Cliff, G., Scholl, M. C., Francis, M., Duffy, C. A. J. and Martin, A. P. (2001) Sex-biased dispersal of great white sharks – In some respects, these sharks behave more like whales and dolphins than other fish. Nature 412, 139–140. Pratt, H. L. and Carrier, J. C. (2001) A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environmental Biology of Fishes 60, 157–188. Ryman, N., Utter, F. and Laikre, L. (1995) Protection of intraspecific biodiversity of exploited fishes. Reviews in Fish Biology and Fisheries 5, 417–446. Sambrook, J. and Russell, D. W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. Schindler, D. E., Essington, T. E., Kitchell, J. F., Boggs, C. and Hilborn, R. (2002) Sharks and tunas: Fisheries impacts on predators with contrasting life histories. Ecological Applications 12, 735–748. Schrey, A. W. and Heist, E. J. (2002) Microsatellite markers for the shortfin mako and cross-species amplification in Lamniformes. Conservation Genetics 3, 459–461. Schrey, A. W. and Heist, E. J. (2003) Microsatellite analysis of population structure in the shortfin mako (Isurus oxyrinchus). Canadian Journal of Fisheries and Aquatic Sciences 60, 670–675. Shivji, M. S., Pank, M., Natanson, L. J., Kohler, N. E. and Stanhope, M. J. (2008) Case study: Rapid species identification of pelagic shark tissues using genetic approaches. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Smith, P. J. (1986) Low genetic variation in sharks (Chondrichthyes). Copeia 1986, 202–207. Utter, F. M. (1991) Biochemical genetics and fishery management – An historical perspective. Journal of Fish Biology 39, 1–20.

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Vos, P., Hogers, R., Bleeker, M., Reijans, M., Vandelee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M. and Zabeau, M. (1995) AFLP – A new technique for DNA fingerprinting. Nucleic Acids Research 23, 4407–4414. Waples, R. S. (1998) Separating the wheat from the chaff – Patterns of genetic differentiation in high gene flow species. Journal of Heredity 89, 438–450. Ward, R. D. and Grewe, P. M. (1994) Appraisal of molecular-genetic techniques in fisheries. Reviews in Fish Biology and Fisheries 4, 300–325. Ward, R. D., Woodwark, M. and Skibinski, D. O. F. (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. Journal of Fish Biology 44, 213–232. Weber, J. L. (1990) Informativeness of human (dC–dA)n and (dG–dT)n polymorphisms. Genomics 7, 524–530. Wilson, A. C., Cann, R. L., Carr, S. M., George, M., Gyllensten, U., Helm-Bychowski, K. M., Higuchi, G., Palumbi, S. R., Prager, E. M., Sage, R. D. and Stoneking, M. (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biological Journal of the Linnaean Society 26, 375–400. Wright, S. (1969) Evolution and the Genetics of Populations. Vol. 2. The Theory of Gene Frequencies. University of Chicago Press, Chicago, IL.

Chapter 29

Case Study: Rapid Species Identification of Pelagic Shark Tissues Using Genetic Approaches Mahmood S. Shivji, Melissa Pank, Lisa J. Natanson, Nancy E. Kohler and Michael J. Stanhope

Abstract The morphological similarity of many commercially exploited sharks, coupled with the widespread practice of delivering often difficult-to-identify carcasses and detached fins to port, has made the collection of shark fishery catch data on a species-specific basis nearly impossible. We report here on the utility of a simple, rapid, accurate, and relatively inexpensive genetic assay for identifying tissues and body parts from five shark species (silky, dusky, sandbar, shortfin mako, longfin mako) commonly encountered in pelagic fisheries. Key words: species identification, shark fins, genetic identification, pelagic sharks, PCR primers, shark DNA.

Introduction Because of the different life-history characteristics of individual shark species, the effective management and conservation planning of shark fisheries worldwide will require the collection of catch data on a species-specific basis. A major impediment to obtaining these data, however, is the significant problem of accurate species identification of many sharks caught as both target species and bycatch. These problems arise from the morphological similarities of many fished sharks (Castro et al., 1999), the common fishery practice of head, tail, and most fin removal from the landed sharks, leaving carcasses that are difficult to identify (Castro, 1993), and the escalation in the practice of shark “finning,” in which only the fins are kept. Accurate identification of the species-of-origin of detached shark fins is often extremely difficult, requiring careful examination by experts. The development of alternative methods for accurate discrimination of carcasses, fins, and flesh would dramatically improve species identification. Although molecular genetics provides such methods (Martin, 1993; Heist and Gold, 1998), their routine application Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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for shark identification in fisheries management and conservation does not yet occur, and awaits the availability of even simpler and more rapid techniques. To this end we have developed a streamlined, simple genetic approach for identifying several pelagic shark species using polymerase chain reaction (PCR) primers that are species specific in their ability to amplify shark DNA (Shivji et al., 2002). The use of PCR methods offers the advantage of requiring only very tiny pieces of samples (⬍10 mg) for analysis. Here we present three case studies demonstrating the utility of this approach for rapid and accurate shark species identification.

General methods Detailed molecular methods and data on PCR primer design, sequences, and testing for species specificity are reported in Pank et al. (2001) and Shivji et al. (2002). Speciesspecific PCR primers for silky shark (Carcharhinus falciformis, Carcharhinidae), dusky shark (C. obscurus), sandbar shark (C. plumbeus), shortfin mako (Isurus oxyrinchus, Lamnidae), and longfin mako (I. paucus) were designed based on DNA sequence differences in the nuclear ribosomal internal transcribed spacer 2 (ITS2) locus among these species. Species identification was achieved by amplifying shark genomic DNA using three primers in a single PCR reaction: (1) a shark species-specific forward primer and (2) two shark “universal” (i.e., non-species specific) forward and reverse primers with annealing sites located at the 3⬘-end of the 5.8S and 5⬘-end of the 28S ribosomal RNA genes flanking the ITS2 locus, respectively (Fig. 29.1). Each species-specific primer was designed to anneal to the ITS2 locus in a location that would yield an easily recognizable (i.e., upon agarose gel electrophoresis), diagnostic-sized PCR fragment when used in amplification reactions with the universal primers.

Case studies Case study 1: A carcharhinid shark originally tagged as a silky was recaptured by a longliner and identified as a dusky by a fishery observer. PCR amplification of the DNA from the recaptured “dusky” shark using both dusky and silky species-specific primers produced a diagnostic-sized PCR fragment unambiguously identifying the animal as a silky (Fig. 29.2(a), lane 9). 1 5.8S rDNA

S

L 28S rDNA

ITS2

2 Fig. 29.1 Relative annealing sites for shark universal primers and, for example, the shortfin and longfin mako species-specific primers in shark ribosomal DNA. 1 and 2: shark universal primers. S and L: shortfin mako and longfin mako species-specific primers, respectively.

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Case study 2: Sandbar and dusky sharks are morphologically similar (Castro, 1993) and can be difficult to distinguish, especially when young. A shark identified as a dusky based on morphology during a fisheries-independent National Marine Fisheries Service shark survey was genetically identified as a sandbar using both dusky and sandbar speciesspecific primers (Fig. 29.2(b)). Case study 3: A mako (species uncertain) captured by a commercial charter vessel was brought to us for identification by the vessel captain. The shark was described as having “mushy flesh,” an apparent characteristic of longfin makos. Genetic testing using both

* 1 2 3 4 M 5 6 7 8 9 M

⫹ Sk

Dk

(a) * 1 2 3 4 M 5 6 7 8 M

⫹ Sb

Dk

(b) Fig. 29.2 Agarose gel results demonstrating identification of sharks using species-specific dusky, silky, and sandbar PCR primers. * denotes lanes containing PCR products from sharks of mistaken identity. ⫹ arrows mark PCR products generated from the two shark universal primers. (a) Lanes 1–4: species-diagnostic PCR products from four known dusky sharks (Dk arrow); lanes 5–8: species-diagnostic PCR products from four known silky sharks (Sk arrow); lane 9: PCR results show the shark identified as a dusky on recapture to be a silky. (b) Lanes 1–4: species-diagnostic PCR products from four known sandbar sharks (Sb arrow); lanes 5–7: species-diagnostic PCR products from three known dusky sharks (Dk arrow); lane 8: PCR results show the shark identified as a dusky to be a sandbar. M lanes are molecular size standards.

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* 1 2 3 4 M 5 6 7 8 9 M

⫹

SF

LF

Fig. 29.3 Agarose gel results demonstrating identification of unknown mako (lane marked by asterisk) using species-specific shortfin and longfin mako primers. Lanes 1–4: species-diagnostic PCR products from four known shortfin makos (SF arrow); lanes 6–9: species-diagnostic PCR products from four known longfin makos (LF arrow); lane 5: PCR results identify the unknown mako as a shortfin mako. ⫹ and M as in Fig. 29.2 legend.

longfin and shortfin mako species-specific primers unambiguously identified the shark as a shortfin mako (Fig. 29.3).

Conclusions Our genetic approach for identifying pelagic shark tissues is streamlined and simple, facilitating rapid and unambiguous species identification. It currently requires approximately 8–10 hours for analysis of up to 80 samples per trained person. Incorporation of appropriate automated DNA isolation methods could increase the rate of analysis by threefold. After DNA isolation from the sample, the assay is streamlined by requiring only PCR without the commonly used additional steps of restriction enzyme analysis of the PCR fragment to produce a species-diagnostic DNA “fingerprint,” or DNA sequencing. Species identification is based simply on detection of an amplified, diagnostic-sized DNA fragment. With the development of species-specific primers for additional sharks (Chapman et al., 2003; Abercrombie et al., 2005; Clarke et al., 2006; M. S. Shivji, unpublished data), this technique is routinely being used to help NOAA’s Office for Law Enforcement detect illegal exploitation of protected species (e.g., Shivji et al., 2005) and characterize the international shark fin trade (Shivji et al., 2002; Clarke et al., 2006). The relatively simple and rapid technology employed should also make this technique amenable for shipboard use on fisheries enforcement and research vessels.

Acknowledgments We thank the US National Marine Fisheries Service, Hai Stiftung/Shark Foundation, and PADI Foundation International for supporting this research.

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References Abercrombie, D. L., Clarke, S. C. and Shivji, M. S. (2005) Global-scale genetic identification of hammerhead sharks: Application to assessment of the international fin trade and law enforcement. Conservation Genetics 6, 775–788. Castro, J. I. (1993) A Field Guide to the Sharks Commonly Caught in Commercial Fisheries of the Southeastern United States. NOAA Technical Memorandum NMFS-SEFSC-338. NOAA/NMFS, Silver Spring, MD. Castro, J. I., Woodley, C. M. and Brudeck, R. L. (1999) A Preliminary Evaluation of the Status of Shark Species. FAO Fisheries Technical Paper No. 380. FAO, Rome, Italy. Chapman, D., Abercrombie, D., Douady, C., Pikitch, E., Stanhope, M. and Shivji, M. (2003) A streamlined, bi-organelle, multiplex PCR approach to species identification: Application to global conservation and trade monitoring of the great white shark, Carcharodon carcharias. Conservation Genetics 4, 415–425. Clarke, S. C., Magnussen, J. E., Abercrombie, D. L., McAllister, M. and Shivji, M. S. (2006) Identification of shark species composition and proportion in the Hong Kong shark fin market based on molecular genetics and trade records. Conservation Biology 20, 201–211. Heist, E. J. and Gold, J. R. (1998) Genetic identification of sharks in the US Atlantic large coastal shark fishery. Fisheries Bulletin 97, 53–61. Martin, A. P. (1993) Application of mitochondrial DNA sequence analysis to the problem of species identification of sharks. In: Conservation Biology of Elasmobranchs (ed. S. Branstetter). NOAA Technical Report NMFS 115. NOAA/NMFS, Silver Spring, MD, pp. 53–59. Pank, M., Stanhope, M., Natanson, L., Kohler, N. and Shivji, M. (2001) Rapid and simultaneous identification of body parts from the morphologically similar sharks Carcharhinus obscurus and Carcharhinus plumbeus (Carcharhinidae) using multiplex PCR. Marine Biotechnology 3, 231–240. Shivji, M., Clarke, S., Pank, M., Natanson, L., Kohler, N. and Stanhope, M. (2002) Genetic identification of pelagic shark body parts for conservation and trade-monitoring. Conservation Biology 16(4), 1036–1047. Shivji, M. S., Chapman, D. D., Pikitch, E. K. and Raymond, P. W. (2005) Genetic profiling reveals illegal international trade in fins of the great white shark, Carcharodon carcharias. Conservation Genetics 6, 1035–1039.

Chapter 30

Stock Structure of the Blue Shark (Prionace glauca) in the North Atlantic Ocean Based on Tagging Data Nancy E. Kohler and Patricia A. Turner

Abstract Members of the Cooperative Shark Tagging Program of the National Marine Fisheries Service tagged 91,450 blue sharks (Prionace glauca) in the North Atlantic Ocean from 1962 to 2000, and 5,410 of these sharks were recaptured, for an overall recapture rate of 5.9%. Blue sharks made frequent trans-Atlantic crossings from the western to eastern regions, and were shown to move between most areas; the mean distance traveled was 857 km, and the mean time at liberty between tagging and recapture was 0.9 year. Shark size, sex ratio, maturation, and movements for each region are discussed, as are sex and size segregation patterns. North Atlantic blue sharks are believed to constitute a single stock, and a better understanding of their complex movements, life-history strategies, and population structure is needed to develop informed management of this open ocean species. Key words: blue shark, migration, movements, North Atlantic, stock structure, tagging, recapture.

Introduction The blue shark (Prionace glauca, Carcharhinidae) is the world’s widest-ranging chondrichthyan. It has a circumglobal distribution and occurs in tropical, subtropical, and warmtemperate seas, including the Mediterranean (Bigelow and Schroeder, 1948; Aasen, 1966; Nakano and Stevens, 2008). In the Atlantic, the blue shark is considered the most abundant pelagic shark (Bigelow and Schroeder, 1948; McKenzie and Tibbo, 1964), and ranges from Newfoundland to Argentina in the west, from Norway to South Africa in the east (Bigelow and Schroeder, 1948; Compagno, 1984), and over the entire mid-Atlantic (Aasen, 1966). It is oceanic-epipelagic, but also frequents fringe-littoral habitats (Compagno, 1984); it occurs from the surface to at least 600 m depth (Carey and Scharold, 1990) and demonstrates tropical submergence (Compagno, 1984; Nakano, 1994). Movements of the blue shark are strongly influenced by water temperature (Vas, 1990; Nakano and Seki, 2003), Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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and the species undergoes seasonal latitudinal migrations on both sides of the North Atlantic (Stevens, 1976; Casey, 1985; Aires-da-Silva et al., 1996) and South Atlantic (Hazin et al., 1990), and in the North Pacific (Nakano, 1994). Blue sharks are a major proportion of bycatch in high-seas longline and drift-net fisheries in all the world’s oceans (Castro et al., 1999), as well as in coastal longline and tuna purse-seine fisheries of the North Pacific (Nakano and Seki, 2003). A recent approximation suggests that they represent 17% by weight of the overall Hong Kong fin market (Clarke et al., 2006). Over the last decade, several nations with high-seas longline fleets in the Atlantic have begun to specifically target blue sharks for their fins and meat (Mejuto et al., 2002; Neves dos Santos et al., 2002). This shift in fishing effort by the Spanish fleet has been driven by favorable changes in the international market and the implementation of highly restrictive measures regulating swordfish catches in the Atlantic Ocean. During the early years of the Portuguese swordfish longline fishery, which developed after 1986 in the North Atlantic, blue sharks were discarded at sea and not recorded in logbooks or included in catch statistics. However, in the 1990s, landings and logbook reports of pelagic sharks have increased, reflecting a change in the marketing of these species and implementation of new ICCAT reporting resolutions (Neves dos Santos et al., 2002). Stock assessments have been conducted on blue shark populations around the world. In the North Pacific and tropical Indian Ocean, assessments of the impact of high-seas fisheries on blue shark stocks indicated that historic catch levels did not have a significant influence on the blue shark populations in some areas (Nakano and Seki, 2003). In the North Atlantic Ocean, a number of studies have reported conflicting trends in population size using general linear models to produce standardized catch rates from both fisherydependent and fishery-independent catch per unit effort databases. Results have varied from declining (US pelagic longline logbook data: Cortés, 2002; Baum et al., 2003; fishery-independent data: Simpfendorfer et al., 2002), to irregular but apparently stable (Japanese pelagic longline logbook data: Nakano, 1999; US pelagic longline logbook data: Cramer, 1999), to irregular but apparently increasing populations (US recreational data: Babcock et al., 1999; Brown, 1999; Cortés, 2002). Conclusions of a 2004 ICCAT assessment for the North and South Atlantic indicated that current biomass appears to be above the biomass at maximum sustainable yield. However, because the sources of these data series may be limited in time and space, it is difficult to speculate on reliable trends across the entire North Atlantic for this oceanic species and the results are considered preliminary (ICCAT, 2005). In the Atlantic, there is a critical need to compile information on blue shark lifehistory parameters, including the movement patterns of this highly migratory fish. A review of North Atlantic pelagic shark tagging data through 1997 yielded results for 21 species of pelagic sharks from nine distinct studies (Kohler and Turner, 2001). Aside from the Cooperative Shark Tagging Program (CSTP) of the National Marine Fisheries Service, data consisted of 19,814 tagged and 580 recaptured sharks, yielding a return rate of 2.9%. The greatest distances and times at liberty from these studies are 1,072 km and 9.5 years in the Canadian Atlantic (Burnett et al., 1987), 7,871 km and 4.5 years off Ireland (Fitzmaurice and Green, 2000), and 7,176 km and 10.7 years off England (Stevens, 1990). This chapter presents a summary of 39 years of CSTP blue shark tagging data. By analyzing the spatial patterns of sex and size classes, we extend previous analyses and

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revisit hypotheses concerning the migratory movements, mixing, and stock structure of this pelagic shark species in the Atlantic Ocean basin.

Methods Summaries of the history and methods of the CSTP have been published previously (Casey, 1985; Kohler et al., 1998; Kohler and Turner, 2001). Tagging and recapture sizes were recorded as fork length (FL), total length (TL), and/or weight. These sizes were primarily estimated at time of tagging and recapture, but also include actual measurements. All lengths, including those from previously published studies, were converted to fork length in centimeters (cm) using the relationships reported in Kohler et al. (1995). Distance traveled between tagging and recapture sites was determined by straight-line distance. Sizes at maturity were 183 cm FL for males, whereas females pass through a subadult phase from 145 to 185 cm FL (Pratt, 1979). Tagging fork length was used to determine the respective maturity group. To examine regional trends in size and maturation, the North Atlantic, defined as north of the equator, was divided into five geographic areas: northwestern North Atlantic (NWNA; west of 30ºW and north of 25ºN), northeastern North Atlantic (NENA; east of 30ºW and north of 25ºN), Mediterranean Sea (MED; east of 6ºW), southeastern North Atlantic (SENA; east of 40ºW and south of 25ºN), and southwestern North Atlantic (SWNA; west of 40ºW and south of 25ºN, including the Gulf of Mexico). Area boundaries were based solely on tagging distributions, which largely reflect the fishing effort patterns of cooperative taggers and should not be associated with management units at this time.

Results and discussion A total of 91,450 blue sharks were tagged from 1962 to 2000 by fishermen and scientists cooperating with the CSTP. Recreational fishermen, using rod and reel, accomplished the bulk of the tagging (67%), while biologists and commercial fishermen, using primarily longlines and handlines, accounted for most of the remainder. During this period, cooperators returned information on 5,410 recaptured blue sharks for an overall recapture rate of 5.9%. Recreational (55%) and commercial (41%) fishermen were responsible for the majority of the tag returns using rod and reel and longline gear, respectively. Overall, fishermen from 44 countries and island territories returned recapture information on tagged blue sharks; recaptured blue sharks were originally tagged on vessels from 18 different nations. The recapture rate for blue sharks originally captured on rod and reel and for those tagged while free-swimming (no capture gear) was 7%. The recapture rates for fish caught on handlines and longlines were 5.5% and 3.2%, respectively. These recovery percentages may be influenced by differences in gear, gear-specific survival, captain’s experience level, geographic area of tagging, and time at liberty. Distances traveled ranged from 0 to 6,926 km, with a mean distance of 857 km. More than 75% of the sharks were recaptured less than 1,500 km from their tagging location.

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Times at liberty ranged from 1 day to 9.1 years, with a mean of 0.9 year. Overall, 75% were at liberty for less than 2 years.

Distribution of sizes and sex ratios A subset of the total tagging database was created that included only blue sharks with information on size and location. This regional database consisted of 90,478 tagged fish (Table 30.1). Blue sharks tagged in the NWNA consisted primarily of immature fish (juvenile males and juvenile and subadult females) and adult males, with a nearly equal number of each sex (sex ratio of 1:0.8). Thirty-nine percent of the males and 12% of the females were of a mature size. In the NENA, mostly immature fish of both sexes (juvenile males and juvenile and subadult females) and some mature females were tagged, with a total sex ratio heavily favoring females (1:2.1). Only 6% of the males and 23% of the females were of a mature size. The presence of juvenile fish and overall predominance of females in this area have been reported in studies off Norway (Pethon, 1970), Ireland (Fitzmaurice et al., 2005), and England (Tucker and Newnham, 1957; Stevens, 1976, 1990; Vas, 1990). In the MED, tagged blue sharks were primarily small immature fish of both sexes, with more females than males (1:1.5); less than 2% of both sexes were mature. These data indicate that the Mediterranean area serves as a primary nursery ground for the blue shark, and these grounds continue off Portugal and as far north as the Bay of Biscay (Stevens, 1990). Aires-da-Silva et al. (1996, 2008) suggested that the Azorean area also represents an important nursery ground in the spring. In contrast, tagged sharks in the SENA were primarily adults of both sexes; 86% of the males and 84% of the females were mature. This area had an overwhelming predominance of males, with a sex ratio of 1:0.3. The presence of large mature fish and a predominance of males have been reported off Africa (Draganik and Pelezarski, 1983; Castro and Mejuto, 1995). In the SWNA, more mature than immature fish were tagged, with adult males making up the largest percentage. Sixtynine percent of the males and 38% of the females were mature, and the sex ratio was nearly equal (1:0.9). In general, the smallest fish of both sexes were found in the MED (70 cm mean FL), with the next smallest group occurring adjacent to this area in the NENA (125 cm mean FL; Fig. 30.1). More males than females were mature in the NWNA, with the reverse being the case in the NENA. Overall, the largest fish and the highest proportion of mature fish of both sexes were tagged in the southern areas (eastern and western) of the North Atlantic, with the largest mean sizes for males and females (205 and 204 cm FL, respectively) and the highest percentage of mature fish (86% and 84%, respectively) found in the SENA.

Transregional movements A total of 446 blue sharks from the CSTP exhibited transregional movements. Earlier studies showed that blue sharks recaptured from both sides of the Atlantic may return in succeeding years to the area in which they were tagged (Casey, 1985; Stevens, 1990). Therefore, blue sharks recovered in their original tagging areas after various times at liberty may not necessarily imply regional residence.

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Table 30.1 Summary of regional sex, size, and maturity information for 90,478 tagged North Atlantic blue sharks from the Cooperative Shark Tagging Program, 1962–2000.* Area

Sex

NWNA

Combined Male

Maturity stage

Juvenile Adult Female Juvenile Subadult Adult NENA

Combined Male Juvenile Adult Female Juvenile Subadult Adult

MED

Combined Male Juvenile Adult Female Juvenile Subadult Adult

SENA

Combined Male Juvenile Adult Female Juvenile Subadult Adult

SWNA

Combined Male Juvenile Adult Female Juvenile Subadult Adult

N

Mean fork length (cm)

Fork length range (cm)

Sex ratio M:F

86,899 35,034 21,501 13,533 26,426 12,130 11,049 3,247

164 172

31–429 34–429

1:0.8

150

31–396

125 98

30–381 32–255

133

30–381

70 65

30–259 30–259

73

30–251

205 205

60–300 60–292

204

60–242

184 197

46–356 46–306

171

65–305

1,368 380 359 21 796 503 112 181 698 226 223 3 344 324 14 6 1,087 808 110 698 218 9 25 184 426 138 43 95 124 37 40 47

% mature

39

12

1:2.1 6

23

1:1.5 1

2

1:0.3 86

84

1:0.9 69

38

*

Fish of unknown sex are not broken down into maturity sizes. NWNA: northwestern North Atlantic; NENA: northeastern North Atlantic; MED: Mediterranean Sea; SENA: southeastern North Atlantic; SWNA: southwestern North Atlantic.

Trans-Atlantic migrations in this study from northwestern and southwestern Atlantic releases (N ⫽ 4,862) include a total of 214 blue sharks (4.4%) that were recaptured in the NENA, SENA, and MED areas. In contrast, 10 sharks (7.2%) were recovered in the western Atlantic that had been tagged in the eastern Atlantic (N ⫽ 138). Although the number

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Male blue sharks

NWNA (35034)

NENA

(380)

MED

(226)

SENA

(808)

SWNA

(138)

0

50

100

150

200

250

300

350

400

450

Fork length (cm) Female blue sharks

NWNA (26426)

NENA (796)

MED (344)

SENA

(218)

SWNA (124)

0

50

100

150

200

250

300

350

400

450

Fork length (cm) Fig. 30.1 Reported fork lengths of tagged male and female blue sharks from the CSTP, 1962–2000. The boundary of the box closest to zero indicates the 25th percentile, lines within boxes mark the median, and the boundary of the box farthest from zero indicates the 75th percentile. Bars to the right and left of boxes indicate the 10th and 90th percentiles, with outliers shown by dots. The mean reported fork length is indicated by ⫹. The vertical dashed lines show fork length at maturity and reflect a subadult phase for females.

of latter recoveries is small, the higher recapture rate indicates that it is likely that transAtlantic movement patterns are similar in both directions. Other tagging studies have reported on northwestern and southwestern Atlantic returns for blue sharks tagged off England (Stevens, 1990) and Ireland (Fitzmaurice et al., 2005).

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A subset of the recapture database was created that included only blue sharks with sex, size, and location data. This database was analyzed for transregional movements and consisted of 3,941 returns (Fig. 30.2). Of the 3,803 blue sharks tagged in the NWNA that were recaptured, 92% were recovered in the same region, with the balance from the NENA (85), MED (1), SENA (85), and SWNA (143). In the NWNA, more mature fish of both sexes traveled out of their original tagging area than the other life-history stages. Of these fish, more were recovered in the SWNA than in any other area. One adult male tagged in the NWNA was recaptured in the MED. Of the 83 blue sharks tagged in the NENA that were recaptured, 80% remained in the area. Movement to other areas included NWNA (8), SENA (7), SWNA (1), and MED (1). Of the NENA recaptured adults, 50% were recaptured in the southernmost areas. More than 70% of the smaller males and females were re-caught in their original tagging area. One subadult female was recaptured in the MED. All 24 of the recaptured juvenile blue sharks tagged in the MED were caught in the original tagging area. The only recaptured subadult female moved a short distance into the NENA. In the SENA, of the 11 sharks tagged and recaptured, all were adult males and females and 91% were recovered there. The only fish recaptured outside the region was a mature male caught in the NENA. Of the 19 recaptured blue sharks tagged in the SWNA, 6 remained in their original tagging area; movements to the other areas included NWNA (6), NENA (5), and SENA (2). This area had the highest percentage of fish recaptured out of their original tagging area, though the sample size was small. Fifty percent or less of the fish of both sexes and all lifehistory stages were recaptured in the original area, with a higher percentage of the larger males and females traveling to other areas (NWNA and NENA). Other studies support these general movement patterns. Previous analysis of these data showed that in the western North Atlantic, the winter range of the blue shark lies eastward of the Gulf Stream (including the Sargasso Sea), where some fish can be found during all months of the year (Casey, 1985). In April and May, as the shelf waters warm, sharks move shoreward from the Gulf Stream onto the continental shelf from North Carolina to Newfoundland. Female blue sharks (145–185 cm FL; 3- to 5-year olds) arrive on the mating/feeding grounds of the continental shelf in the NWNA in late May and early June, where they interact with adult males (4- to 5-year olds; Casey, 1985). The high incidence of mating scars and the presence of sperm in oviducal glands indicate a primarily summer breeding season for the blue shark, although mating can continue until as late as November off the northeast coast of the United States (Pratt, 1979). After the females are inseminated, the sperm is stored and they move offshore until egg fertilization the following spring (Pratt, 1979). In late summer and fall, most of the blue sharks along the eastern North American coast begin moving south and offshore (Casey, 1982, 1985) to areas off the southeastern United States and into the Caribbean Sea and central, eastern, and southern North Atlantic. In the eastern North Atlantic, there is seasonal north–south movement (from 30° to 50°N) and different patterns of movement for various portions of the population (Stevens, 1976, 1990). Off the southwest coast of England, there are two main movements of blue sharks into the area in summer: A movement of larger females at the beginning of the season

346 Sharks of the Open Ocean

Fig. 30.2 Summary of movements of blue sharks with sex, size, and location information from the CSTP, 1962–2000. Arrows and numbers indicate the movements of individual sharks between and within areas; numbers within circles are sharks tagged and recaptured in the same region. The total number recaptured from each area is: NWNA, 3,803; NENA, 83; MED, 25; SENA, 11; SWNA, 19.

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347

is followed by smaller fish, including more males, by the end of July or early August (modal length 150–160 cm FL), with the latter remaining until about September (Stevens, 1976, 1990). During the summer months, blue sharks travel north to waters off Ireland and Scotland, into the North Sea, and to outer areas of the Baltic Sea, and are found along the west coast of Norway as strays (Aasen, 1966). Small fish (modal length 100–110 cm FL) remain within a relatively confined area and do not take part in the more extensive north–south migration of the larger fish. Blue sharks are present until at least November off northern Spain, after which they may move farther south, possibly as far as the Canary Islands (Stevens, 1976, 1990). Mating of adult males and females is thought to occur in spring and summer between 32º and 35ºN. Adult females, many pregnant, have been found in the area between the African coast, Madeira, and the Canary Islands in the winter months (Aasen, 1966; Stevens, 1990). Limited movement took place between the North Atlantic and the Mediterranean, occurring only three times in this study. Similar results are found in the Irish recreational fisheries data from 1970 to 2001 (Fitzmaurice et al., 2005). Information was also collected on four blue sharks that had crossed the equator into the South Atlantic. Two (one male and one sex unknown) were tagged off the northeast coast of the United States (NWNA) and two (both males) south of the Cape Verde Islands (SENA). Time at liberty was 0.2–1.7 years and distance traveled was 1,737–6,926 km. Additionally, two blue shark recaptures (one male and one female) not part of this analysis were tagged in the NWNA and recaptured off Ascension Island, south of the equator. Stevens (1990) reported one female blue shark that crossed the equator (tagged off the southwest coast of England and recaptured off South America in the South Atlantic) after 3.1 years at liberty.

Summary It is generally believed that most shark species segregate by size and sex during their life history (Strasburg, 1958; Springer, 1960), and the blue shark is no exception. Evidence from tagging studies and catch data suggest distinct seasonal abundances and seasonal latitudinal migrations for discrete portions of the blue shark population. The separation of sexes other than at the time of mating may be an adaptation for females to avoid the dangers associated with male mating behavior (Nakano, 1994). Distribution and movements of this species are strongly influenced by seasonal variations in water temperature, reproductive condition, and availability of prey. This has been documented for blue sharks in the North Atlantic (Tucker and Newnham, 1957; Stevens, 1976; Casey, 1985; Stevens, 1990; Aires-da-Silva et al., 1996; Henderson et al., 2001), in the South Atlantic (Hazin et al., 1990, 1994), in the Pacific (Suda, 1953; Strasburg, 1958; Sciarrotta and Nelson, 1977; Nakano, 1994; Nakano and Nagasawa, 1996; Nakano and Seki, 2003), and in the Indian Oceans (Gubanov and Grigor’yev, 1975). On the basis of tagging data, blue sharks of the North Atlantic constitute a single stock of fish that make frequent west-to-east and east-to-west trans-Atlantic movements. Blue sharks likely utilize the major North Atlantic current systems to accomplish these extensive movements (Stevens, 1976, 1990; Casey, 1985; Fitzmaurice et al., 2005). In addition, this species is segregated by sex and size across vast regions of the Atlantic, with larger, mature fish of both sexes caught in the southern part of their range. The present study found that mean

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size generally decreases with increasing latitude, in accord with findings by Suda (1953), Strasburg (1958), and Nakano (1994) for the North Pacific and by Gubanov and Grigor’yev (1975) for the Indian Ocean. Immature males and females and subadult females dominate the northern regions, with the smallest fish being found in the Mediterranean. Sex ratios of nearly 1:1 are found in the western North Atlantic, and primarily females in the northeastern Atlantic and Mediterranean; males predominate in the southeastern region. Documented seasonal migrations to the higher latitudes occur on both sides of the North Atlantic. These analyses and conclusions are based on tagging data primarily from the northwestern North Atlantic. Sample sizes for the other regions are much smaller, and additional data in these areas are needed. Other investigators have found similar localized results that support a one-stock hypothesis involving a complex reproductive cycle with mating areas in the northwestern North Atlantic and pupping areas in the eastern North Atlantic. Partial exchange occurs between North and South Atlantic waters, but the magnitude and frequency of this movement are unknown. Genetic and stable-isotope studies are needed to further test the single-stock hypothesis. It is imperative that we improve our understanding of the complex movements, life-history strategies, and population structure of the highly migratory blue shark in the Atlantic Ocean so that fishery managers are able to devise valid management schemes to sustainably exploit this important pelagic species.

Acknowledgments We are indebted to the personnel of the Apex Predators Investigation, especially R. Briggs, for her continued support in the CSTP. Our sincere thanks go to the countless volunteer fishermen who released and recaptured sharks in the tagging program. Without their efforts over the years, this research would not have been possible. We are particularly grateful to J. Casey, whose great vision to establish the CSTP many years ago has inspired the tagging of thousands of blue and other species of sharks over the entire Atlantic Ocean. We also thank J. Hoey, L. Natanson, K. Duffy, F. Almeida, and J. Burnett for critical reviews and K. Tougas for providing valuable technical assistance.

References Aasen, O. (1966) Blahaien, Prionace glauca (Linnaeus, 1758). Fisken og Havet 1, 15. Aires-da-Silva, A. A., Silva, H. M. and Erzini, K. (1996) Some Results on the Biology of the Blue Shark, Prionace glauca, in the North Atlantic Based on Data from a Research Cruise of the R/V Arquipelago in Azorean Waters: A Summary Paper. Universidade dos Açores, Horta, Açores, Portugal, 9 pp. Aires-da-Silva, A. A., Ferreira, R. L. and Pereira, J. G. (2008) Case study: Blue shark catch-rate patterns from the Portuguese swordfish longline fishery in the Azores. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Babcock, E. A., Pikitch, E. K. and McAllister, M. K. (1999) Catch rates of blue sharks (Prionace glauca) in the US Atlantic recreational fishery. ICCAT Collective Volume of Scientific Papers 51(6), 1850–1857. Baum, J. K., Myers, R. A., Kehler, D. G., Worm, B., Harley, S. J. and Doherty, P. A. (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299, 389–392.

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Bigelow, H. B. and Schroeder, W. C. (1948) Sharks. In: Fishes of the Western North Atlantic. Part 1. Lancelets, Cyclostomes, Sharks (eds. A. E. Parr and Y. H. Olsen). Sears Foundation for Marine Research, New Haven, CT, pp. 59–546. Brown, C. A. (1999) Standardized catch rates of four shark species in the Virginia–Massachusetts (US) rod and reel fishery 1986–1998. ICCAT Collective Volume of Scientific Papers 51(6), 1812–1820. Burnett, C. D., Beckett, J. S., Dickson, C. A., Hurley, P. C. F. and Iles, T. D. (1987) A summary of releases and recaptures in the Canadian large pelagic fish tagging program, 1961–1986. Canadian Data Report of Fisheries and Aquatic Sciences 673, 99. Carey, F. G. and Scharold, J. (1990) Movements of blue sharks (Prionace glauca) in depth and course. Marine Biology 106, 329–342. Casey, J. G. (1982) Blue shark, Prionace glauca. Species synopsis. In: Ecology of the Middle Atlantic Bight Fish and Shellfish (eds. M. D. Grosslein and T. Azarovitz). Monograph 15, Fish Distribution, MESA New York Bight Atlas. New York Sea Grant, Albany, NY, pp. 45–48. Casey, J. G. (1985) Trans-Atlantic migrations of the blue shark: A case history of cooperative shark tagging. In: World Angling Resources and Challenges (ed. R. H. Stroud). International Game Fish Association, Ft. Lauderdale, FL, pp. 253–267. Castro, J. A. and Mejuto, J. (1995) Reproductive parameters of blue shark Prionace glauca and other sharks in the Gulf of Guinea. Marine and Freshwater Research 46, 967–973. Castro, J. I., Woodley, C. M. and Brudek, R. L. (1999) A Preliminary Evaluation of the Status of Shark Species. FAO Fisheries Technical Paper No. 380. FAO, Rome, Italy, 72 pp. Clarke, S. C., Magnussen, J. E., Abercrombie, D. L., McAllister, M. K. and Shivji, M. (2006) Identification of shark species composition and proportion in the Hong Kong shark fin market based on molecular genetics and trade records. Conservation Biology 20(1), 201–211. Compagno, L. J. V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 2. Carcharhiniformes. FAO Fisheries Synopsis No. 125. FAO, Rome, Italy, pp. 521–524. Cortés, E. (2002) Catches and catch rates of pelagic sharks from the northwestern Atlantic, Gulf of Mexico, and Caribbean. ICCAT Collective Volume of Scientific Papers 54(4), 1164–1181. Cramer, J. (1999) Large pelagic logbook catch rates for sharks. ICCAT Collective Volume of Scientific Papers 51(6), 1842–1848. Draganik, B. and Pelezarski, W. (1983) The occurrence of the blue shark, Prionace glauca (L.), in the North Atlantic. In: Reports of the Sea Fisheries Institute, Vol. 19. Sea Fisheries Institute, Gdynia, Poland, pp. 61–75. Fitzmaurice, P. and Green, P. (2000) Results from tagging of blue shark in Irish waters. Offprint from The Irish Scientist Millennium Year Book. Central Fisheries Board, Mobhi Boreen, Glasnevin, Dublin, Ireland. Fitzmaurice, P., Green, P., Keirse, G., Kenny, M. and Clarke, M. (2005) Stock discrimination of the blue shark, based on Irish tagging data. ICCAT Collective Volume of Scientific Papers 58(3), 1171–1178. Gubanov, Ye. P. and Grigor’yev, V. N. (1975) Observations on the distribution and biology of the blue shark Prionace glauca (Carcharhinidae) of the Indian Ocean. Journal of Ichthyology 15, 37–43. Hazin, F. H. V., Couto, A. A., Kihara, K., Otsuka, K. and Ishino, M. (1990) Distribution and abundance of pelagic sharks in the southwestern equatorial Atlantic. Journal of the Tokyo University of Fisheries 77(1), 51–64. Hazin, F. H. V., Boeckman, C. E., Leal, E. C., Lessa, R. P. T., Kihara, K. and Otsuka, K. (1994) Distribution and relative abundance of the blue shark, Prionace glauca, in the southwestern equatorial Atlantic Ocean. Fishery Bulletin 92, 474–480. Henderson, A. C., Flannery, K. and Dunne, J. (2001) Observations on the biology and ecology of the blue shark in the north-east Atlantic. Journal of Fish Biology 58, 1347–1358. Kohler, N. E. and Turner, P. A. (2001) Shark tagging: A review of conventional methods and studies. Environmental Biology of Fishes 60, 191–223.

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Kohler, N. E., Casey, J. G. and Turner, P. A. (1995) Length–weight relationships for 13 species of sharks from the western North Atlantic, 1995. Fishery Bulletin 93, 412–418. Kohler, N. E., Casey, J. G. and Turner, P. A. (1998) NMFS Cooperative Shark Tagging Program, 1962–93: An atlas of shark tag and recapture data. Marine Fisheries Review 60, 1–87. ICCAT (2005) Report of the 2004 Inter-sessional Meeting of the ICCAT Sub-committee on By-catches: Shark Stock Assessment, Tokyo, Japan, 14–18 June 2004. ICCAT Collective Volume of Scientific Papers 58(3), 799–890. McKenzie, R. A. and Tibbo, S. N. (1964) A morphometric description of the blue shark (Prionace glauca) from the Canadian Atlantic waters. Journal of the Fisheries Research Board of Canada 21, 865–866. Mejuto, J., Garcia-Cortes, B. and de la Serna, J. M. (2002) Preliminary scientific estimations of by-catches landed by the Spanish surface longline fleet in 1999 in the Atlantic Ocean and Mediterranean Sea. ICCAT Collective Volume of Scientific Papers 54(4), 1150–1163. Nakano, H. (1994) Age, reproduction and migration of blue shark in the North Pacific. Bulletin of the National Research Institute of Far Seas Fisheries 31, 141–256. Nakano, H. (1999) Updated standardized CPUE for pelagic sharks caught by Japanese longline fishery in the Atlantic Ocean. ICCAT Collective Volume of Scientific Papers 51(6), 1796–1803. Nakano, H. and Nagasawa, K. (1996) Distribution of pelagic elasmobranchs caught by salmon research gillnets in the North Pacific. Fisheries Science 62(6), 860–865. Nakano, H. and Seki, M. P. (2003) Synopsis of biological data on the blue shark, Prionace glauca Linnaeus. Bulletin of the Fisheries Research Agency 6, 18–55. Nakano, H. and Stevens, J. D. (2008) The biology and ecology of the blue shark, Prionace glauca. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Neves dos Santos, M., Garcia, A. and Pereira, J. G. (2002) A historical review of the by-catch from the Portuguese surface long-line swordfish fishery: Observations on blue shark (Prionace glauca) and short-fin mako (Isurus oxyrinchus). ICCAT Collective Volume of Scientific Papers 54(4), 1333–1340. Pethon, P. (1970) Occurrence of the great blue shark Prionace glauca in Norwegian waters. Rhizocrinus 1(3), 177–188. Pratt Jr., H. L. (1979) Reproduction in the blue shark, Prionace glauca. Fishery Bulletin 77, 445–470. Sciarrotta, T. C. and Nelson, D. R. (1977) Diel behavior of the blue shark, Prionace glauca, near Santa Catalina Island, California. Fishery Bulletin 75(3), 519–528. Simpfendorfer, C. A., Hueter, R. E., Bergman, U. and Connett, S. M. H. (2002) Results of a fishery-independent survey for pelagic sharks in the western North Atlantic, 1977–1994. Fisheries Research 55, 175–192. Springer, S. (1960) Natural history of the sandbar shark, Eulamia milberti. Fishery Bulletin 61, 1–38. Stevens, J. D. (1976) First results of shark tagging in the Northeast Atlantic, 1972–1975. Journal of the Marine Biological Association of the United Kingdom 56, 929–937. Stevens, J. D. (1990) Further results from a tagging study of pelagic sharks in the Northeast Atlantic. Journal of the Marine Biological Association of the United Kingdom 70, 707–720. Strasburg, D. W. (1958) Distribution, abundance, and habits of pelagic sharks in the central Pacific Ocean. Fishery Bulletin 58, 335–361. Suda, A. (1953) Ecological Study of the Blue Shark (Prionace glauca Linne’). South Sea Area Fisheries Research Laboratory Report 26(Suppl. 1), 1–11. Tucker, D. W. and Newnham, C. T. (1957) The blue shark Prionace glauca breeds in British seas. Annual Magazine of Natural History 12(10), 673–688. Vas, P. (1990) The shark catch of 1978 in the western English Channel. Environmental Biology of Fishes 29, 315–317.

Chapter 31

Why Are Bayesian Methods Useful for the Stock Assessment of Sharks? Murdoch K. McAllister, Ellen K. Pikitch and Elizabeth A. Babcock

Abstract Ichthyologists alerted fishery managers three decades ago to the low reproductive capacity of sharks and their high susceptibility to overexploitation. In many instances, it remains impossible to confidently apply current fisheries stock assessment methods to shark populations and to provide compelling scientific evidence to motivate conservation action where it is needed. This is due to a variety of reasons, including a paucity of biological data and fishery-independent times-series of abundance for sharks, as well as substantial differences in biology between sharks and other exploited fish species. In this chapter, we review some of the goals and requirements of stock assessment methods for sharks, and outline why Bayesian methods may be useful. When used in conjunction with existing modeling methods, the Bayesian approach could help strengthen the scientific support needed for designing precautionary fishery management policies for sharks. Key words: Bayesian, stock assessment, demographic methods, catch per unit effort, population dynamics, Bayes’ theorem.

Introduction Recent increases in catches of sharks in many coastal and pelagic fisheries have raised concerns about their conservation (NMFS, 1996; Walker, 1998; Camhi, 2008). These concerns have stimulated increased interest in assessing the status of shark populations and developing management approaches to prevent further decline and to rehabilitate depleted populations (NMFS, 1998; Punt and Walker, 1998; Punt et al., 2000; Kleiber et al., 2001; Babcock and Nakano, 2008). Compared with teleosts, sharks have received little attention until recently from fishery managers and stock assessment scientists. Information that is crucial for the conservation of many shark populations is currently lacking, and the reproductive, ecological, and migratory characteristics of many sharks are poorly known. Furthermore, few reliable time-series of observations on the abundance of shark populations have been collected, and few stock assessment methods have been developed and applied to provide scientific advice to fishery managers. Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Research over the last 30 years has alerted fishery managers to the low reproductive capacity of sharks and their susceptibility to overexploitation (e.g., Holden, 1977; Sminkey and Musick, 1995; Cortés, 1999). However, it is difficult, using the existing sparse data, to confidently apply current assessment methods to provide compelling scientific evidence that will motivate conservation action where it is needed. This chapter reviews some of the goals and requirements of stock assessment methods for sharks, and outlines why Bayesian methods can be appropriate for these assessments. We argue that, when used in conjunction with other modeling methods, such as demographic modeling (Cortés, 1999, 2008; Au et al., 2008), Bayesian stock assessments of sharks could help to strengthen the scientific support needed for designing precautionary fishery management policies for sharks (FAO, 1995).

What should be the main goal of stock assessment for sharks? According to Hilborn and Walters (1992), the main goal of stock assessment should be to inform decision makers of the potential consequences of different management actions. This requires using the best available scientific information and data to evaluate the potential consequences of alternative management actions, communicating these consequences to managers, and informing managers of important uncertainties (Hilborn et al., 1993; McAllister and Kirkwood, 1998a). Table 31.1 lists considerations in each of the various phases of a stock assessment that may help in formulating scientific advice for fisheries management. Given the general paucity of appropriate data and biological research on pelagic sharks, and because data collection and analysis are not well coordinated among countries, meeting even a portion of these considerations would be onerous for most shark stocks. In several instances, however, stock assessments of a shark population or sets of populations have been undertaken, and will be in the future, because of recently formulated research initiatives (e.g., Anonymous, 1999) and legislative requirements, and because of the substantial economic and other values at stake in the conservation and exploitation of sharks (NMFS, 1996, 1998; Walker et al., 2008). The next section briefly reviews some of the stock assessment methods that have been applied to sharks.

How has advice been provided for shark fishery management? Demographic analysis One of the most common analytical methods applied to help formulate shark fishery management advice is demographic analysis (Krebs, 1985; Fowler, 1988; Cortés, 1999, 2008; Au et al., 2008). This requires as inputs some of the basic population dynamics parameters, such as the rate of natural mortality at each life stage, the duration of each life stage (e.g., immature and mature), and the fecundity or number of newly born offspring produced per female at each age. All of these inputs should be those expected when there is no density dependence, that is, when population abundance is very low. Quite conveniently, this approach does not require time-series observations of relative abundance. A variety of

Table 31.1 Some considerations that may be taken into account in the various phases of a stock assessment. Considerations

Compile basic biological information and data on the following

Life-history parameters Migratory behavior Stock structure Critical habitats Ecological relationships

Compile fishery data on the following

Fleet fishing strategies and gear selectivity Annual catch and bycatch removals Annual target fishing effort (from fisheries targeted on the stock) and nontarget fishing effort (from fisheries targeted on other fish stocks that happen to catch the stock being assessed) Historic trends in catchability Catch-rate indices and fishery-independent indices of abundance Mark-and-recapture data if such experiments have been carried out

Construct appropriate PDMs and estimate their parameters

Which types of models should be adopted? (e.g., biomass dynamic or age-structured, single stock or multistock, spatially aggregated or disaggregated) Which parameter estimation methods should be applied? What assumptions should be used in fitting models to data? For example, how has catchability changed over time for a given catch-rate series? Does catchability vary systematically with abundance (Walters and Maguire, 1996)?

Develop and apply methods for quantitative policy evaluation to address the following questions

How well are current management measures meeting management objectives? • Are current fishing practices “sustainable”? • What are the recent trends in abundance and what is current abundance? • What are the recent trends in fishing mortality rates? Are proposed management options likely to meet management objectives? • What needs to be done to prevent further decline, and to promote stock recovery? • Are the proposed policy measures sufficiently precautionary, and robust to uncertainty? What is the probability (risk) of exceeding a limit reference point with the alternative policy measures? • This question presumes that biological and/or economic limit reference points can be specified. • This question could be answered using Monte Carlo simulations available in risk analysis packages such as Crystal Ball or in Bayesian stock assessment software such as that described herein.

Why Are Bayesian Methods Useful for Stock Assessment?

Phases of a stock assessment

353

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quantitative methods, ranging from very simple life table analysis (Krebs, 1985; Begon et al., 1996) to more sophisticated demographic methods (Cortés, 1999, 2008; Quinn and Deriso, 1999; Au et al., 2008; Smith et al., 2008), can be applied to these various inputs. Most commonly, these methods are applied to estimate the intrinsic rate of increase of the population, r, which reflects the maximum per capita rate of increase in the population at very low population abundance (Krebs, 1985; Begon et al., 1996). This parameter provides a simple indication of a population’s potential resilience to exploitation. Because of uncertainties and natural random variation, probabilistic estimates that accounted for estimation uncertainties would be most useful for management purposes (Cortés, 1999). Demographic analyses can also indicate the realized rate of increase of a population, if additional sources of mortality such as exploitation are also present (Cortés, 1999; Au et al., 2008; Smith et al., 2008). The measures provided, however, typically reflect predictions under equilibrium conditions and thus cannot be used to assess current trends in abundance or the potential population responses to changes in fishery regulations. This method can also be used as an independent check for other types of population analysis. Perhaps the most difficult aspect of this method is obtaining estimates of the rates of natural mortality at age. However, for some sharks, mark-and-recapture experiments have been successfully executed and can be applied for this purpose (NMFS, 1998; Punt et al., 2000).

Fitting surplus production models to times-series of observations on relative abundance Nonequilibrium surplus production models (SPMs) have been applied to many teleosts and marine mammals. These models can be used to estimate recent trends in abundance and to evaluate the potential consequences of alternative management actions. However, SPMs have been applied in relatively few instances with sharks (Xiao, 1995; NMFS, 1996, 1998; Cortés et al., 2002; Babcock and Nakano, 2008). Some have questioned whether models that aggregate age groups into one category of exploitable biomass can adequately model the population dynamics of long-lived, latematuring individuals. Extensive simulation work conducted by the International Whaling Commission (IWC) indicated that age-aggregated models often perform no worse than age-disaggregated models in evaluations of proposed management procedures for harvesting of whale populations (IWC, 1992), which are similar in life-history characteristics to many shark species. However, in the IWC work, the stock assessment models were fitted to absolute abundance data, rather than relative abundance data (the latter are more common), and it is questionable whether the results can be generalized to shark fisheries management. In simulation evaluations of stock assessment methods applied to moderately longlived teleosts, when the data to which models were fitted included relative abundance data, simple, age-aggregated models have sometimes been found to provide better estimation performance than age-disaggregated models (Ludwig and Walters, 1985; Punt, 1993). This is partly because age-structured models require more parameters than SPMs, so there is more scope for errors in parameter inputs to cause bias in estimates of abundance. Estimation of SPM parameters requires a time-series of total catch removals, preferably from the start of the fishery, and at least one time-series of relative abundance. Despite their simplicity, SPMs can be used to formulate sophisticated management procedures that

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incorporate limit and target biological reference points such as maximum sustainable yield (MSY), as well as risk-based reference points (McAllister and Kirkwood, 1998b; McAllister et al., 2001). They cannot be used to evaluate the potential consequences of management measures that affect specific age groups, such as gear restrictions, size limits, and marine reserves in pupping and nursery areas.

Age-structured, length-structured, or stage-structured modeling The approach of fitting age-structured and length-structured (or, more generally, stagestructured) models to relative abundance indices and tagging and/or catch-age or length frequency data has been even more rarely applied to sharks than the above-mentioned approaches (Punt and Walker, 1998; Punt et al., 2000; Kleiber et al., 2001; Cortés et al., 2002; Apostolaki, 2003). This is primarily because of onerous data requirements, since considerable age- or stage-structured information and data on the population and fishery need to be obtained. If such data were available, it would appear to be the most desirable approach for shark stock assessment. Many sharks are long-lived and migratory and can be caught in different fisheries at different life stages (e.g., Punt et al., 2000; Apostolaki, 2003). While age-aggregated models permit only the exploration of the effects of alternative total catch removals from the population, age-structured models permit a more refined analysis. Bias in the evaluation of historic trends in abundance can be reduced because differential shifts in age structure due to variability in recruitment and differential vulnerability at age to exploitation can be accounted for with age-structured models. The impacts on potential future stock abundance of changes in regulations for different fisheries that affect different life stages of a population, for example, changes in gear regulations and time and area closures that affect different age classes, can be evaluated (Apostolaki, 2003). However, it is generally more difficult to quantitatively evaluate uncertainties in parameter values and model structure with more complex models (McAllister and Kirchner, 2002).

Some problems encountered with conventional assessment methods As indicated above, there are a number of difficulties in applying the various stock assessment methods to sharks. Five of these are outlined here.

Compiling basic biological and fishery data For most shark populations, few resources have been allocated for stock assessment research. Bias in estimates of abundance can be reduced by utilizing time-series of fisheriesindependent indices of abundance from standardized surveys, yet because of the large costs of implementing such surveys, few time-series exist. This leaves only time-series of commercial catch rates for both target and bycatch fisheries for sharks, and in many cases even these are not available. Because of uncertainty in how catchability may change with abundance or other factors, the catch-rate data, even when standardized for the seasons and areas fished, can be very difficult to interpret and sometimes unusable as indices of abundance. Catch-rate data may not be usable as abundance indices if the following processes influence catch rates: the extent of gear saturation by target species, which can affect catch rates

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of bycatch species such as sharks and can change owing to changes in target species abundance; changes in the species groupings targeted; changes in gear and electronic technology; systematic temporal changes in the areas fished; and range contraction of the target population. If any of these conditions affect catchability, conventional stock assessment methods cannot be used with these data. In some cases, it may be appropriate to consider a variety of different shapes for the catch per unit effort (CPUE) versus abundance relationship (Walters and Maguire, 1996) and different hypotheses about the impact of learning and gear technology advances on catchability (Babcock and McAllister, 2004). Tagging data obtained through mark-and-recapture experiments, though costly, have proven useful in evaluating the population biology of some sharks (Punt et al., 2000). For the southern Australian school shark (Galeorhinus galeus, Triakidae), these have permitted a sophisticated age-structured stock assessment that modeled separately the males and females in two subpopulations with different migratory patterns through eight different spatial zones (Walker et al., 2008).

Integrating different types of data and results For many shark fisheries, only a few sources of information are available, such as several life-history parameters and some catch and catch-rate data. Not enough information and data may be available for an age-structured stock assessment, but sufficient information may be available to implement the surplus production and demographic methods separately. For various reasons highlighted below, it would be of interest to integrate both sets of results in providing management advice. Yet conventional assessment methodologies do not provide a systematic approach for doing so.

Reconciling contradictory data, information, and results Very often in stock assessment, different sources of information or results from different methods yield contradictory results (Schnute and Hilborn, 1993). For example, different time-series of abundance observations might reflect contradictory trends in abundance, or different methods might provide very different estimates of stock status and resilience to exploitation (Cortés et al., 2002). Current methods do not provide systematic approaches to dealing with such ambiguities. The provision of management advice can then become controversial, with the most appropriate action depending on which analysis or source of information is applied. For sharks, this is particularly problematic, because data are sparse and obtaining additional data series to resolve contradictions would be difficult. Moreover, because sharks are slow-growing and long-lived and have low fecundity, it would often take too long to gather further data that might help to resolve these ambiguities. Experimental management approaches that might be feasible for shorter-lived, more fecund species (Sainsbury, 1988) may be unacceptable for sharks.

Thoroughly accounting for uncertainty Monte Carlo simulation methods are commonly applied in a variety of approaches to account for uncertainty in the values of stock assessment model parameters (Restrepo et al.,

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1992; Punt and Hilborn, 1997; McAllister et al., 1999). However, relatively little attention has been devoted to dealing with structural uncertainties, that is, uncertainties in the structural formulation of models (Patterson, 1999; McAllister and Kirchner, 2002). For example, there is often considerable uncertainty over the functional form for the quantity of catchability. In some situations we may ask whether catchability varies systematically with abundance (Walters and Maguire, 1996), or whether catchability increases only with advances in gear technology, learning, and increased targeting of sharks due to increased demand for shark fins. If only catch and relative abundance data are present, structurally different models for catchability could be formulated for these two alternative hypotheses (McAllister and Kirchner, 2002). The sparseness of data would not permit them to be incorporated into a single nested model because the resulting model would be overparameterized. It is often the case that the best management action to take depends on which of the models is applied. Without formal scientific guidance on how to give weightings to results from the alternative assumptions, managers usually apply their own weightings. These may deviate considerably from scientific considerations. For example, managers weighted outcomes from 20 alternative model specifications for school shark equally without considering the scientific plausibility of the alternatives (Punt et al., 2000). In other instances, managers have discarded the most pessimistic alternatives without giving any explicit justification (e.g., ICCAT, 1999). Scientists need more empirically based methods to evaluate scientific evidence so that they can in turn provide more empirically based objective guidance to managers on how to weight such alternatives (Butterworth et al., 1996; McAllister et al., 1999; McAllister and Kirchner, 2002).

Conveying uncertainty in a meaningful way to decision makers It is becoming more widely recognized that uncertainties in model results should be conveyed using probabilities and decision analytic methods (Francis and Shotton, 1997; McAllister et al., 1999). Although the basic elements of decision analysis have been widely applied in many stock assessments, different methods have been applied to calculate probabilities for model parameters, with varying degrees of statistical rigor (see McAllister et al., 1999, for a review). Data for sharks are generally more difficult to interpret (e.g., because sharks may be captured as bycatch rather than as target species) than data for other species, and thus uncertainty in decision making is a particularly serious issue for shark fisheries management. Therefore, decision analytic methods that deal explicitly with uncertainty are well suited for shark management. In stock assessments for sharks, probabilistic and decision analytic approaches have been applied only recently (NMFS, 1996, 1998; Punt and Walker, 1998; Cortés et al., 2002; Walker et al., 2008).

How should uncertainty be dealt with in stock assessment? Decision analytic theory (Raiffa, 1968; Berger, 1985) suggests that the following elements be applied in dealing with uncertainty in stock assessment: identify alternative plausible hypotheses; evaluate the evidence in support of each hypothesis; and use decision tables with mathematical probabilities.

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Identify alternative plausible hypotheses In stock assessment, there are two general types of hypotheses (or scenarios). The first involves alternative structural forms for the population dynamics model (PDM) for past and future processes. For example, there may be different hypotheses about how catchability has changed over time or is related to population abundance (Walters and Maguire, 1996). Each alternative needs to be clearly specified in mathematical form. Although there is an infinite set of alternative structural forms that can be considered, it is often practical to consider a relatively small set of structural alternatives, perhaps no more than a halfdozen plausible alternatives. It is important to include biologists, industry members, and fishery managers familiar with the fishery or ones similar to it in the identification of alternative structural models. The second type involves alternative values for the parameters in a PDM. For example, alternative values for the intrinsic rate of increase, r, in the Schaefer model could be treated as alternative hypotheses. These alternative hypotheses could be in continuous terms (0.05
r1  0.10; 0.10
r2  0.15) or discrete terms (r1  0.075; r2  0.125). They can be thought of as conjectures about past and future states of the resource. Thus, we can have hypotheses for the values of parameters for historic events as well as for future events, such as future annual deviates from a stock-recruit function.

Evaluate the weight of evidence in support of each hypothesis The first step is to specify prior probabilities (see below) for the alternative hypotheses (HA) based on expert judgment. If each HA is deemed to be equally likely before the data for the population in question are analyzed, then each HA may be given equal probability. Meta-analysis methods that combine data from several different populations have recently been developed as a means to synthesize such data and to develop prior probabilities for model parameters (Gelman et al., 1995; Liermann and Hilborn, 1997; Prévost et al., 2003). Some assessment approaches have been designed to update the prior probabilities assigned to the alternative hypotheses by fitting the model to the data and providing posterior probabilities for each HA (Patterson, 1999; Parma, 2001; McAllister and Kirchner, 2002). The posterior probabilities for each HA are taken as the weight of all evidence in support of the alternative hypotheses. Fairly even posterior probabilities across hypotheses convey considerable uncertainty; very high probabilities over a very concentrated range of hypotheses indicate much less uncertainty.

Use decision tables without mathematical probabilities In data-limited fisheries such as most shark fisheries, where observations that could be used to evaluate the plausibility of alternative states of nature (e.g., alternative structural forms for the PDM) are scarce, the use of decision tables without mathematical probabilities could also be considered. Decision tables are constructed with columns for the possible (unknown) states of nature, rows for the potential management actions, and the cells filled in with, for example, the economic value of each action for each state of nature. These types of decision tables and corresponding decision criteria are available from decision

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theory (e.g., Raiffa, 1968). Applications in fisheries are included in Food and Agriculture Organization (FAO, 1995), Seijo et al. (1998), Defeo and Seijo (1999), and Seijo and Caddy (2000). When probabilities for the plausibility of alternative states of nature cannot be obtained, the Maximin and Minimax regret criteria (Resnik, 1987) could provide a workable framework for making decisions using the precautionary approach for shark fisheries management. The Maximin criterion ignores the most optimistic scenarios and associated best-case scenario rewards. It suggests choosing the action that yields the maximum value in the worst-case scenario. This criterion expresses a high degree of risk aversion. The Minimax regret criterion is less pessimistic and suggests choosing the action that is expected to lead to the minimum “regret,” where regret is defined as the difference between the value of a particular action for a particular state of nature and the value of the best action for that state of nature.

Bayesian methods The assignment of probability to alternative values for a parameter reflects the key feature of Bayesian statistics. Methods have also been recently developed and applied to compute Bayesian probabilities (credibilities) for structurally different stock assessment models (Patterson, 1999; Parma, 2001; McAllister and Kirchner, 2002). These methods are based on one fundamental axiom of probability: Bayes’ theorem (Bayes, 1763). This axiom allows the calculation of the probability that a hypothesis is true from all available data.

Bayes’ theorem Bayes’ theorem, or a simpler statement of it, Bayes’ rule (below), has three fundamental components: a prior probability for each of the alternative hypotheses, a probability of the data, and the posterior probability. In Bayesian analysis we start with the prior probability, Prior Prob(HA is true) – this reflects what we know or believe about the relative credibility of an HA before evaluating new data. For example, if for some species we knew very little about the value for the parameter r in the Schaefer model, we would start out with a relatively flat or “noninformative” distribution for that parameter. In contrast, if there were some indication of a most likely range of values based on knowledge of the reproductive biology of the species (McAllister et al., 2001), or other similar populations (Gelman et al., 1995; Liermann and Hilborn, 1997), then the prior distribution would be an informative one with a rounded peak about the most likely values. A key assumption in the use of the prior probability is that it reflects the credibility of alternative hypotheses before the current data are analyzed and is completely independent of the potential information contained in the data. There is often a risk that knowledge of existing data feeds into the development of priors, making the priors more informative than they should be, and not independent of the data used in Bayes’ theorem. There is also a risk, when priors are formulated from expert judgment, that the experts are overly certain in their knowledge and supply priors that are too narrow. This can be dangerous, because it can prevent data from overriding the biased priors (McAllister and Kirkwood, 1998b). In shark

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stock assessment, this risk is especially pertinent because the data most commonly obtained are already sparse, imprecise, and relatively uninformative. Thus care is needed in the formulation of priors (see Punt and Hilborn, 1997; McAllister and Kirkwood, 1998a). The next step is to identify a functional form for the probability distribution for the stock assessment data for the population in question that could result if one of the HA were true (i.e., the probability of the data). For example, if the hypotheses pertained to the mean length of fish of a given age in a population, and the data were observations of individual fish sampled at random from the population, then we might expect the observations to be normally distributed. The probability of obtaining the data if HA were true would then be given by the normal density function. Each observation would have its own normal distribution, and we would use this to calculate the probability of obtaining the observation assuming the hypothesized value for the mean and standard deviation of the normal distribution for hypothesis HA. The likelihood of the entire set of observations, or “data,” would be the product of the probabilities for each of the individual observations. In summary, the prior comes from inferences from other similar populations or, in the case of SPMs, from demographic information on the population in question (McAllister et al., 2001). We then update that information with the stock assessment data for the population in question. The posterior probability reflects what we have learned about a set of alternative hypotheses after evaluating a set of data. We start with the prior, then analyze the data, and our updated understanding is reflected in the posterior probability distribution. This updating occurs through the application of Bayes’ rule: Posterior Prob(HA is true from data)  Prior Prob(HA is true)  Prob(obtaining the data if HA were true) This formulation suggests why Bayesian statistics are so useful. They allow the calculation of the probability that a hypothesis is true using diverse sources of data. For example, in an application of Bayesian methods to Baltic salmon (Salmo salar, Salmonidae) stock assessment, a prior probability density function (pdf) for the slope parameter in the Beverton–Holt stock-recruit function was obtained from a meta-analysis of stock-recruit data for nine Atlantic salmon populations (Michielsens, 2003). A prior pdf for the carrying capacity of Baltic salmon was obtained by an evaluation of Baltic salmon biologists’ knowledge of the attributes of Baltic salmon rivers. Tagging data on Baltic salmon were analyzed to compute posterior distributions for catchability, natural mortality rates, and homing rates from the sea to the river at different sea ages. The results of these analyses served as prior pdfs in the stock assessment model of population dynamics of Baltic salmon. This model was fitted to the time-series of juvenile salmon abundance data to produce a posterior distribution for the stock assessment model parameters. In shark fisheries, the requirements for estimating posterior probabilities are: a PDM can be formulated; estimable parameters are identified; prior pdfs can be specified for the parameters; and data are compiled to which the model can be fitted. It is essential that the data compiled contain information to help estimate the model parameters. For example, relative abundance indices must show responses (e.g., declines) to catch removals and variations in response to variations in catch removals. It may be that the data by themselves might not be sufficient for parameter estimation (e.g., a monotonic decline in catch rates),

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but when combined with moderately informative priors for one or more of the estimated parameters in Bayes’ theorem, the combination of the data and the prior provide posterior outputs with sufficient precision to help guide fisheries management decisions (McAllister et al., 2001). More informative data for shark stock assessment could come from a multiyear mark-and-recapture experiment, if resources were available (Punt et al., 2000). Bayes’ theorem can also be applied to compute a posterior probability for structurally different models given the available data (Raftery and Richardson, 1996; Patterson, 1999; Parma, 2001; McAllister and Kirchner, 2002).

Example: National Marine Fisheries Service assessment of Atlantic coastal sharks The National Marine Fisheries Service (NMFS) stock assessment of large coastal sharks (LCSs) in 1996 used a variety of data and applied different assessment tools to provide management advice (NMFS, 1996). This assessment and the ones that followed in 1998 and 2002 illustrate well why Bayesian methods can be so useful for stock assessment of sharks (NMFS, 1998; Cortés et al., 2002). The 1996 assessment included several critical elements.

Demographic analysis of life-history parameters to estimate the intrinsic rate of increase, r Estimates of the key life-history parameters for demographic analysis were obtained for two carcharhinid sharks, blacktip (Carcharhinus limbatus) and sandbar (C. plumbeus). Point estimates of r were calculated using some alternative combinations of values for the parameters, since the values were not known precisely. In addition, to more thoroughly account for uncertainty, probability distributions for the parameters were constructed, and a Monte Carlo simulation was applied to compute a probability distribution for r. Each of the different demographic analyses suggested that the values for r for blacktip and sandbar sharks were centered around 0.1 (Fig. 31.1).

SPMs to estimate r, recent trends in stock size, and the potential effectiveness of different recovery plans Several different catch-rate series were available for use as indices of relative abundance for the species grouped as LCS. An SPM was fitted to these data using a maximum likelihood method to estimate the value of r and carrying capacity (K). The value obtained was 0.26, more than twice as high as those obtained in the demographic analyses. The differing estimates suggested large uncertainty in r, yet this was neglected in the policy analysis and provision of management advice. Despite the apparent uncertainty in the estimate of r, only the more optimistic estimate was applied.

A Bayesian stock assessment of Atlantic large coastal sharks The Bayesian methods applied in the 1998 and 2002 assessments of LCSs overcame these shortcomings by combining the demographic evaluation with surplus production estimation

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Blacktip

Prior density

Sandbar

0

0.05

0.10

0.15

0.20

0.25

0.30

0.35

0.40

Intrinsic rate of increase Fig. 31.1 Prior density functions for the intrinsic rate of increase for blacktip and sandbar sharks based on a Monte Carlo analysis of life-history parameters that determines the intrinsic rate of increase for these two species. Log-normal density functions have been used to describe the results of the Monte Carlo simulations.

and modeling (McAllister et al., 2001). The surplus model parameter estimation was conducted in these two assessments using the various commercial, recreational, and fisheryindependent catch-rate series for LCSs. This time, however, a prior probability distribution was constructed for the parameters of the SPM (e.g., r and K ). At first, noninformative (flat) prior probabilities for r and K were applied. After fitting the model to the catch-rate data, it was found that many different combinations of values for r and K fit the data almost equally well. In particular, low values of K and high values of r fit the data, as well as high values of K and low values of r. Additionally, the posterior probability distribution for r was quite flat, suggesting that the catch-rate data did not enable precise estimation of r and that the estimate of 0.26 in the 1996 assessment was imprecise. Bayesian analysis using Monte Carlo methods similar to those applied in the 1996 demographic analysis was applied in the 1998 assessment to construct prior probability distributions for r for blacktip and sandbar sharks. These were combined to formulate a prior for r for the combined stock of LCSs. It also allowed combining this prior with catchrate data to produce a posterior probability distribution for the SPM parameters, r and K. Because the prior distribution produced for the demographic analysis supported values over a limited range, mainly between 0.05 and 0.15 (consistent with these sharks’ low reproductive potential), the resulting posterior distribution for r and K was much more confined than the one without the prior from demographic analysis. Furthermore, the values of r provided by the Bayesian estimation became consistent with knowledge and data about the reproductive biology and life history of LCSs. The resulting posterior probability distribution for r and K was then used in a decision analysis to evaluate the potential consequences of alternative recovery plans. By integrating the relatively uninformative catch-rate data that showed a monotonic decline, which before had suggested a high value for r, with the informative prior for r, the Bayesian approach reconciled sources of information that in the previous assessment appeared to be contradictory. Furthermore, the incorporation of key sources of uncertainty in

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a probabilistic decision analysis of management options permitted the adoption of a precautionary approach.

Recommendations for learning Bayesian stock assessment methods Applying Bayesian methods to shark stock assessment requires knowledge of basic probability theory. The Ecological Detective (Hilborn and Mangel, 1997) is a useful primer for the application of Bayesian methods, and articles by Punt and Hilborn (1997) and McAllister and Kirkwood (1998a) present the main ideas of Bayesian stock assessment. Although some of the very simplest applications can be implemented in spreadsheets, most stock assessment applications are more computationally intensive owing to the number of parameters to be estimated. Computing requirements can also be onerous if one wants to compute posterior probabilities for structurally different models (McAllister and Kirchner, 2002). If there are more than a few parameters to estimate, then Monte Carlo methods for Bayesian parameter estimation are often needed. Several software packages can be used for Bayesian stock assessment, which include the Monte Carlo methods needed to numerically integrate posterior distributions for complex, multiparameter models. These include the freely available WinBUGS (www.mrc-bsu .cam.ac.uk/bugs/winbugs/contents.shtml), which is perhaps the easiest and the most commonly applied Bayesian software (Meyer and Millar, 1999; Link et al., 2002; Mantyniemi and Romakkaniemi, 2002). There is a growing literature describing Bayesian modeling in WinBUGS, including SPM applications (Meyer and Millar, 1999), potential biases in parameter estimates in state-space models (Cunningham, 2002), Bayesian mark–recapture, generalized linear modeling and hierarchical modeling (Link et al., 2002; Mantyniemi and Romakkaniemi, 2002; Prévost et al., 2003), and Bayesian data imputation (Clarke, 2003). AD Model Builder (Otter Research, Sidney, British Columbia, Canada) is a computationally efficient program that has been applied to stock assessment problems with very large numbers of uncertain parameters; it also has an in-built Markov Chain Monte Carlo (MCMC) algorithm to integrate the posterior density function. Bayesian stock assessment and decision analysis software for SPMs has been developed by several of the authors (Babcock and McAllister, 2003) and is downloadable for free from the catalog of stock assessment software at ICCAT (www.iccat.es). This software applies importance sampling rather than MCMC. Key considerations regarding some hazards and limitations of using the Bayesian approach are: If subjective judgment is applied to formulate prior pdfs for model parameters, then • caution is required to avoid the use of narrow priors, and the sensitivity of model out-

•

puts to alternative specifications for priors should always be undertaken to evaluate the impact of priors on estimates of abundance, fishing mortality rates, and fisheries management reference points (McAllister and Kirkwood, 1998a, b). The diagnostics developed for each Bayesian method should always be computed and evaluated to assess whether the results obtained from the Bayesian application have

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converged and have acceptable statistical properties before the methods can be considered for providing management advice (Spiegelhalter et al., 2003). Using models with incorrect structural assumptions (e.g., about catchability or densitydependent processes) will produce incorrect stock assessment results and faulty fisheries management advice whether the method is Bayesian or non-Bayesian. It is therefore important in all stock assessments of sharks to evaluate the sensitivity of results to plausible alternative structural forms of the assessment models employed and to convey the results of these evaluations to fisheries managers. If results are sensitive to structural uncertainty, it is recommended that they be reported in decision table format to facilitate their incorporation in management decisions (McAllister and Kirchner, 2002).

Conclusions Because pelagic sharks are vulnerable to overexploitation, it is crucial that fisheries scientists be able to provide advice on how to manage the fisheries that impact them. However, the requirements for informative catch and abundance data series in conventional stock assessment methods to permit the estimation of the key population parameters of sharks are prohibitive in most instances, because of the lack of availability of such time-series for most shark populations. In contrast, Bayesian stock assessment methods offer an approach when demographic information and catch and relative abundance data for at least the most recent decades of the fishery are available (McAllister et al., 2001; Apostolaki, 2003; ICCAT, 2005). By incorporating such biological information and data in a probabilistic framework, Bayesian stock assessment methods provide the probabilistic basis necessary to implement a precautionary approach for the management of shark fisheries (FAO, 1995).

Acknowledgments This work was made possible by a grant from The David and Lucile Packard Foundation and by the Pew Charitable Trusts through a grant to the Pew Institute for Ocean Science. We thank Jack Musick, Gerry Scott, Joe Powers, Shelley Clarke, Merry Camhi, Geoff Kirkwood, and many others for their helpful discussions. Shelley Clarke provided helpful comments on an early draft, and André Punt offered extensive comments in his review of the manuscript. We thank an anonymous reviewer for helpful comments that improved parts of the manuscript.

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Gelman, A., Carlin, J., Stern, H. and Rubin, D. (1995) Bayesian Data Analysis. Chapman & Hall, Boca Raton, FL. Hilborn, R. and Mangel, M. (1997) The Ecological Detective: Confronting Models with Data. Princeton University Press, Princeton, NJ. Hilborn, R. and Walters, C. J. (1992) Quantitative Fisheries Stock Assessment: Choice, Dynamics, and Uncertainty. Chapman & Hall, New York. Hilborn, R., Pikitch, E. K. and Francis, R. C. (1993) Current trends in including risks and uncertainty in stock assessment and harvest decisions. Canadian Journal of Fisheries and Aquatic Sciences 50, 874–880. Holden, M. J. (1977) Elasmobranchs. In: Fish Population Dynamics (ed. J. A. Gulland). John Wiley & Sons, London, UK, pp. 187–216. ICCAT (1999) ICCAT Collective Volume of Scientific Papers 49(2). ICCAT (2005) Report of the 2004 Inter-sessional Meeting of the ICCAT Sub-committee on By-catches: Shark Stock Assessment. ICCAT Collective Volume of Scientific Papers 58(3), 799–890. IWC (1992) Report of the Scientific Committee. Annex D (Management Procedures). Report of the International Whaling Commission 42, 87–136. Kleiber, P., Takeuchi, Y. and Nakano, H. (2001) Calculation of Plausible Maximum Sustainable Yield (MSY) for Blue Shark (Prionace glauca) in the North Pacific. Administrative Report H-0102. Southwest Fisheries Science Center, NMFS, La Jolla, CA. Krebs, C. J. (1985) Ecology: The Experimental Analysis of Distribution and Abundance, 3rd edn. Harper & Row, New York. Liermann, M. and Hilborn, R. (1997) A hierarchic Bayesian meta-analysis. Canadian Journal of Fisheries and Aquatic Sciences 9, 1976–1984. Link, W. A., Cam, E., Nichols, J. D. and Cooch, E. G. (2002) Of BUGS and Birds: Markov chain Monte Carlo for hierarchical modelling in wildlife research. Journal of Wildlife Management 66(2), 277–291. Ludwig, D. and Walters, C. J. (1985) Are age-structured models appropriate for catch–effort data? Canadian Journal of Fisheries and Aquatic Sciences 42, 1066–1072. Mantyniemi, S. and Romakkaniemi, A. (2002) Bayesian mark–recapture estimation with an application to a salmonid smolt population. Canadian Journal of Fisheries and Aquatic Sciences 59, 1748–1758. McAllister, M. K. and Kirchner, C. H. (2002) Accounting for structural uncertainty to facilitate precautionary fishery management: Illustration with Namibian orange roughly. In: Targets, Thresholds, and the Burden of Proof in Fisheries Management (ed. M. Mangel). Bulletin of Marine Science 70(2)(special volume), 499–540. McAllister, M. K. and Kirkwood, G. P. (1998a) Bayesian stock assessment: A review and example application using the logistic model. ICES Journal of Marine Science 55, 1031–1060. McAllister, M. K. and Kirkwood, G. P. (1998b) Using Bayesian decision analysis to help achieve a precautionary approach to managing newly developing fisheries. Canadian Journal of Fisheries and Aquatic Sciences 55, 2642–2661. McAllister, M. K. Starr, P. J., Restrepo, V. R. and Kirkwood, G. P. (1999) Formulating quantitative methods to evaluate fishery-management systems: What fishery processes should be modelled and what trade-offs should be made? ICES Journal of Marine Science 56(6), 900–916. McAllister, M. K., Pikitch, E. K. and Babcock, E. A. (2001) Using demographic methods to construct Bayesian priors for the intrinsic rate of increase in the Schaefer model and implications for stock rebuilding. Canadian Journal of Fisheries and Aquatic Sciences 58(9), 1871–1890. Meyer, R. and Millar, R. B. (1999) BUGS in Bayesian stock assessments. Canadian Journal of Fisheries and Aquatic Sciences 56, 1078–1086.

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Michielsens, C. (2003) Bayesian Decision Theory for Fisheries Management of Migratory Species with Multiple Life Histories. Ph.D. thesis, Imperial College London, London, UK. National Marine Fisheries Service (NMFS) (1996) Report of the Shark Evaluation Workshop. Southeast Fisheries Science Center, NMFS, Miami, FL. National Marine Fisheries Service (NMFS) (1998) Report of the Shark Evaluation Workshop. Southeast Fisheries Science Center, NMFS, Panama City, FL. Parma, A. M. (2001) Bayesian approaches to the analysis of uncertainty in the stock assessment of Pacific halibut. In: Incorporating Uncertainty into Fisheries Models (eds. J. M. Berkson, L. L. Kline and D. J. Orth). American Fisheries Society, Bethesda, MD, pp. 111–132. Patterson, K. R. (1999) Evaluating uncertainty in harvest control law catches using Bayesian Markov chain Monte Carlo virtual population analysis with adaptive rejection sampling and including structural uncertainty. Canadian Journal of Fisheries and Aquatic Sciences 56, 208–221. Prévost, E., Parent, E., Crozier, W., Davidson, I., Dumase, J., Gudbergsson, G., Hindarg, K., McGinnityh, P., MacLeani, J. and Sættem, L. M. (2003) Setting biological reference points for Atlantic salmon stocks: Transfer of information from data-rich to sparse-data situations by Bayesian hierarchical modelling. ICES Journal of Marine Science 60(6), 1177–1193. Punt, A. E. (1993) The comparative performance of production-model and ad hoc tuned VPA based feedback-control management procedures for the stock of Cape hake off the west coast of South Africa. In: Risk Evaluation and Biological Reference Points for Fisheries Management (eds. S. J. Smith, J. J. Hunt and D. Rivard). Publication No. 120. NRC Research Press, Ottawa, Ontario, Canada, pp. 283–299. Punt, A. E. and Hilborn, R. (1997) Fisheries stock assessment and decision analysis: The Bayesian approach. Reviews in Fish Biology and Fisheries 7, 35–63. Punt, A. E. and Walker, T. I. (1998) Stock assessment and risk analysis for the school shark (Galeorhinus galeus) off southern Australia. Marine and Freshwater Research 49, 719–731. Punt, A. E., Pribac, R., Walker, T. I., Taylor, B. L. and Prince, J. D. (2000) Stock assessment of school shark, Galeorhinus galeus, based on a spatially explicit population dynamics model. Marine and Freshwater Research 51, 205–220. Quinn, T. J. and Deriso, R. B. (1999) Quantitative Fish Dynamics. Oxford University Press, Oxford, UK. Raftery, A. E. and Richardson, S. (1996) Model selection via GLIB. In: Bayesian Biostatistics (eds. D. A. Berry and D. K. Dalene). Marcel Dekker, New York, pp. 321–353. Raiffa, H. (1968) Decision Analysis: Introductory Lectures on Choices Under Uncertainty. Addison-Wesley, Reading, MA. Resnik, M. D. (1987) Choices: An Introduction to Decision Theory. University of Minnesota Press, Minneapolis, MN. Restrepo, V. R., Hoenig, J. M., Powers, J. E., Baird, J. W. and Turner, S. C. (1992) A simple simulation approach to risk and cost analysis, with applications to swordfish and cod fisheries. Fishery Bulletin 90, 736–748. Sainsbury, K. (1988) The ecological basis of multispecies fisheries, and management of a demersal fishery in tropical Australia. In: Fish Population Dynamics: The Implications for Management (ed. J. A. Gulland), 2nd edn. Wiley, Chichester, UK, pp. 349–382. Schnute, J. T. and Hilborn, R. (1993) Analysis of contradictory data sources in fish stock assessments. Canadian Journal of Fisheries and Aquatic Sciences 52, 2063–2077. Seijo, J. C. and Caddy, J. F. (2000) Uncertainty in bio-economic reference points and indicators of marine fisheries. Marine and Freshwater Research 51, 477–483. Seijo, J. C., Defeo, O. and Salas, S. (1998) Fisheries Bio-economics: Theory, Modelling and Management. FAO Fisheries Technical Paper No. 368. FAO, Rome, Italy, 108 pp.

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Sminkey, T. R. and Musick, J. A. (1995) Demographic analysis of the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic. Fishery Bulletin 94, 341–347. Smith, S. E., Au, D. W. and Show, C. (2008) Intrinsic rates of increase in pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Spiegelhalter, D., Thomas, A. and Best, N. (2003) WinBUGS Version 1.4. User Manual. MRC and Imperial College of Science, Technology and Medicine, London, UK (www.mrc-bsu.cam. ac.uk/bugs). Walker, T. I. (1998) Can shark resources be harvested sustainably? Marine and Freshwater Research 49, 553–572. Walker, T. I., Taylor, B. L., Brown, L. P. and Punt, A. E. (2008) Embracing movement and stock structure for assessment of Galeorhinus galeus harvested off southern Australia. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Walters, C. J. and Maguire, J. J. (1996) Lessons for stock assessment from the northern cod collapse. Reviews in Fish Biology and Fisheries 6, 125–137. Xiao, Y. (1995) Stock Assessment of the School Shark Galeorhinus galeus (Linnaeus) off Southern Australia by Schaefer Production Model. SharkFAG Document No. SS/95/D2. Australian Fisheries Management Authority, Canberra, Australian Capital Territory, Australia, 58 pp.

Chapter 32

Embracing Movement and Stock Structure for Assessment of Galeorhinus galeus Harvested off Southern Australia Terence I. Walker, Bruce L. Taylor, Lauren P. Brown and André E. Punt

Abstract Galeorhinus galeus – the school or soupfin shark – is a long-lived, low-productivity species in the family Triakidae that undertakes extensive movements and exhibits complex stock structure. While this widely distributed, temperate-water species is usually characterized as a coastal bentho-pelagic species, it also occurs well off the continental shelf and behaves as an oceanic-pelagic species. Experience with stock assessment of the species off southern Australia has demonstrated that the application of spatially aggregated models can lead to highly uncertain results, despite the availability of catch data covering the 70-year history of the fishery, catch per unit effort data for part of this history, and estimates of parameters that take account of the species’ demography and selectivity characteristics of the fishing gear. To address these high levels of uncertainty, the results from a fine-spatial-scale simulation model of shark movement dynamics based primarily on subjective judgments are included in an agebased and spatially structured fishery assessment model. By allowing for spatial and stock structure and using tagging data for estimation purposes, the production of pups at the start of 1997 is estimated to be 12–18% of the 1927 level. This is a markedly less uncertain range than that obtained using a spatially aggregated model and ignoring the tagging data, which estimated the 1994 mature biomass to be 15–46% of the 1927 level. Past analyses of tag release–recapture data demonstrated the relevance of the movement dynamics to stock assessment. The current method for estimating movement rates among broad zones of the fishery off southern Australia provides a quantitative basis for developing hypotheses of movement. Key words: Galeorhinus galeus, Triakidae, school shark, soupfin shark, tagging, movement, stock structure, stock assessment, mortality, selectivity, growth, model, tag and recapture.

Introduction Galeorhinus galeus (Triakidae) occurs widely in temperate waters of the world in several genetically isolated populations (Ward and Gardner, 1997). Over its range, the species Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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is known variously as school shark (southern Australia and New Zealand), soupfin shark (west coast of North America and South Africa), vaalhaai (South Africa), tiburón vitamínico and tiburón trompa de cristal (Argentina and Uruguay), and cação-bico-de-cristal (Brazil). In the Northeast Atlantic, it is variously called tope (United Kingdom), requin-hâ (France), perna de moça and cação perna de moça (Portugal), and cação (Azores) (Compagno, 1984; Walker, 1999a). Galeorhinus galeus is characterized as a coastal bentho-pelagic species (Compagno, 1984), but it has several features characteristic of oceanic-pelagic species, including the occurrence of individual animals well off the continental shelf (Stevens and Wayte, 1999) and long oceanic movements. Of 541 reported tag recaptures from 2,686 tag releases off southern Australia during 1990–1999, about 100 recaptures of both sexes had displacements of greater than 1,000 km. Of the animals released in southern Australia during 1990–1999, 10 had been recovered from New Zealand by December 1999 (Brown et al., 2000) and 15 had been recovered by December 2005 (unpublished data). One Australian-tagged female released in the Great Australian Bight was recaptured 3,500 km away between the North and South Islands of New Zealand after 4.1 years, released again, and then recaptured off Australia 2,600 km away 2.8 years later (unpublished data). Of the 3,950 animals released in New Zealand (Hurst et al., 1999), 26 have been recovered from southern Australia (Brown et al., 2000). One New Zealand-tagged animal recaptured off southern Australia had a displacement of 4,940 km (Hurst et al., 1999). In the Northeast Atlantic (Holden and Harrod, 1979; Stevens, 1990), animals tagged off England and Ireland have been recaptured as far away as north of Iceland (2,461 km), the Canary Islands (2,526 km), and the Azores. From 136 individuals tagged on the West Coast of North America, 2 released off California were recaptured off British Columbia (1,609 km), and 4 other recaptures were made 121–306 km from their tag release positions (Herald and Ripley, 1951). The shark fishery of southern Australia targets Mustelus antarcticus and, to a lesser extent, G. galeus, but small quantities of several other species are taken as bycatch. The catch is taken mostly by gill nets, but longlines are also used. Regular catches of G. galeus taken by commercial fishers using gill nets that stand with a height of about 2 m on the seabed of the continental shelf suggest the animals spend considerable time near the seabed. This was confirmed by tagging 46 large animals in the southern Australian population with “archival” tags, of which 15 had been recovered by the end of 2000; these tags recorded bathometric pressure and information used for estimating position (West and Stevens, 2001b). The animals from which tags were recovered spent about 80% of their time on the continental shelf. When the sharks are on the continental shelf, they appear to spend most of their time near the seabed, but at night they often ascend, sometimes to the surface. When they move into deeper water, their diving behavior often resembles that of large pelagic sharks and teleosts, as they dive to depths of 660 m during the day before ascending at night (West and Stevens, 2001a, b). The diet of Galeorhinus galeus has been described for southern Australia (Olsen, 1954; Coleman and Mobley, 1984; Walker, 1989b), California (Ripley and Bolomey, 1946), South Africa (Freer, 1992), the Irish Sea (Ellis et al., 1996), the Azores (Morato et al., 2003), and Argentina (Lucifora, 2003). Prey items include both coastal-pelagic and demersal species (Table 32.1). The absence of oceanic-pelagic species in the diet is probably

Table 32.1 Major prey items in the various populations of Galeorhinus galeus. California

South Africa

Irish Sea

Azores

Argentina

Coastal-pelagic teleosts Jack mackerel (Trachurus declivis) Pilchard (Sardinops neopilchardus) Barracouta (Thyrsites atun)

Pacific jack mackerel (Trachurus symmetricus) Pacific sardine (Sardinops sagax)

Cape hake (Merluccius capensis) Southern African pilchard (Sardinops ocellatus)

Atlantic mackerel (Scomber scombrus) Unspecified gadoids (Gadiformes) Atlantic herring (Clupea harengus)

Blue jack mackerel (Trachurus picturatus) Chub mackerel (Scomber japonicus)

Jurel (Trachurus lathami) Anchoíta (Engraulis anchoita) Pejerrey (Odontesthes argentinensis) Anchoa de banco (Pomatomus saltatrix) Saraca (Brevoortia aurea) Palometa (Parona signata) Pampanito (Stromateus brasiliensis) Nata (Peprilus paru)

Demersal teleosts Toothbrush leatherjacket (Acanthaluteres vittiger) Leatherjackets (Meuschenia spp.)

Specklefin midshipman (Porichthys miriaster) Unspecified rockfish

Seabream (Pachymetopon blochii) Carpenter seabream (Argyrozona argyrozona) Unspecified sole (Soleidae) Unspecified mullet (Liza spp.)

Dragonet (Callionymus spp.)

Several sparid species (Sparidae) Boarfish (Capros aper)

Congro (Raneya brasiliensis) Cocherito (Dules auriga) Lisa ( Mugil spp.) Turgo (Pinuipes brasilianus) Pargo blanco (Umbrina canosai) Pescadilla comun (Cynoscion guatucupa)

Coastal cephalopoda Pale octopus (Octopus pallidus)

Unspecified octopus

Unspecified octopus

Curled octopus (Eledone cirrhosa)

Unspecified octopus (Octopodidae)

Pulpito (Octopus tehuelchus)

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(Continued)

371

372

Southern Australia

California

South Africa

Gould’s squid (Nototodarus gouldi) Southern calamari (Sepioteuthis australis) Bragg’s cuttlefish (Sepia braggi)

Unspecified squid

Unspecified squid

Ripley and Bolomey (1946)

Freer (1992)

References Olsen (1954); Coleman and Mobley (1984); Walker (1989b)

Irish Sea

Ellis et al. (1996)

Azores

Argentina

Unspecified cephalopoda (Cephalopoda)

Calamar (Illex argentinus) Calamarete (Loligo sanpaulensis)

Morato et al. (2003)

Lucifora (2003)

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Table 32.1 (Continued).

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because no stomach contents were examined from animals caught in waters beyond the continental shelf. As with oceanic-pelagic sharks such as the blue shark (Prionace glauca) (Casey, 1985; Stevens, 1990; Nakano, 1994; Gubanov and Grigor’yev, 1995) and coastal-pelagic sharks such as the spiny dogfish (Squalus acanthias) (Ford, 1921; Hisaw and Albert, 1947; Compagno, 1984; Nammack et al., 1985; Saunders et al., 1985; Hanchet, 1986; Ketchen, 1986), the stock structure and movement patterns of G. galeus are complex. While some of the complexity of movement allows the sharks to meet food requirements, differences in the patterns of movements between animals of different sex, life-history stage, and, as in G. galeus, reproductive condition suggest that there may be advantages for females in pregnant condition or in the latter stages of the 3-year ovarian cycle in moving to warmer waters during the cooler months of the year (Peres and Vooren, 1991; Walker, 2005). This chapter describes how complex movement patterns and stock structure are accounted for in the stock assessment of G. galeus in the shark fishery of southern Australia. It outlines how an age-based and spatially structured stock assessment model fitted to tag release–recapture and other data while allowing movement of animals among eight separate regions (Fig. 32.1) markedly reduced the uncertainty in estimates of stock depletion. The chapter also describes a separate model used for determining rates of movement among three separate zones (Fig. 32.2).

Stock structure and movement patterns A theory of the movement of G. galeus off southern Australia was first developed from the recapture of sharks tagged and released during 1947–1956 and from anecdotal

Western 129
E Australia

134
E

139
E

143
E

146
E

150
E

South Australia

New South Wales

200

WSA

m

Great Australia Bight 34
S

NSW 37
S

CSA Victoria

SAV

41
S

EBS WBS Tasmania

WT

ET

44
S

Fig. 32.1 Map of eight regions for the spatially structured stock assessment model. CSA: central South Australia; EBS: eastern Bass Strait; ET: eastern Tasmania; NSW: New South Wales; SAV: South Australia–Victoria; WBS: western Bass Strait; WSA: western South Australia; WT: western Tasmania. From Punt et al. (2000b).

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129
E

141
E

150
E

WA New South Wales

SA

200 m

200 m

37
S

BS 41
S Tas

Fig. 32.2 Map of three zones for the movement estimation model. BS: Bass Strait; Tas: Tasmania; WA/SA: Western Australia (127–129ºE) and South Australia combined.

information received from fishers. According to this theory, pregnant sharks move into shallow nursery areas of Tasmania and Victoria to give birth and then, after parturition, move to deeper waters (Fig. 32.1). The adults tend to move inshore during summer, and offshore or north to the warmer waters of New South Wales and South Australia during early winter, before returning south in the spring. The neonates and young juveniles tend to remain in the nursery areas or deeper coastal waters, whereas juveniles of age 2 years or more move to the eastern area of Bass Strait. Older juveniles and subadults distribute more widely across southern Australia waters (Olsen, 1954). Data collected subsequently, as well as the size composition of sharks in the catch after the fishery expanded through South Australia to include the Great Australian Bight, generally support this theory. One exception is the absence of significant catches of G. galeus from the fisheries on the eastern coast of Australia, although this absence might be interpreted as evidence for depletion of a substock occupying this region. Pregnant sharks at most stages of gestation have been observed in waters of the Great Australian Bight, and it appears that they remain here during much of gestation, before returning to eastern Bass Strait and Tasmania to give birth. Recently, it has been found that there is some mixing of tagged animals between southern Australia and New Zealand (Brown et al., 2000). However, genetic differences between animals from the two countries suggest that there is no, or negligible, breeding between these populations (Ward and Gardner, 1997).

Spatially aggregated stock assessment Although it has long been understood that G. galeus has a complex stock structure and movement pattern, apart from one assessment assuming spatially separate stocks in several regions (Prince, 1991), the complexity was ignored in all assessments until 1999. None of the assessments using three types of models applied during 1993–1998 was spatially structured. All assessments used available annual catch data and annual catch per

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unit effort (CPUE) data, and other data were used variously depending on the model. The first type was a biomass dynamics model (Xiao, 1995a). The second type was a delaydifference model, which depended on exogenously determined parameters for natural mortality and growth of the sharks and which was adapted to include stochastic recruitment for risk analysis (Walker, 1995). The third type was an age-based model, which included shark natural mortality, growth, reproduction, and gear selectivity (gill nets of various mesh size and hooks) parameters and assumed levels of interannual variation in pup survival (Punt and Walker, 1998). To account for regional effects in these assessments, region was included as a factor in the standardization of CPUE through generalized linear modeling for deriving a single populationwide time-series of abundance indices. The first CPUE standardization assumed different average catch rates in different regions but the same trend (Xiao, 1995b). Later, this was extended to allow for different time-trends as well as different average annual catch rates in different regions (Punt et al., 2000a). Nevertheless, estimates of stock depletion from all of these spatially aggregated models were highly uncertain (Walker et al., 2000). For example, the range for the estimate of the mature biomass at the start of 1994 was 15–46% of the 1927 level in the spatially aggregated age-based model, adopted for a stock assessment undertaken in 1996 (Punt and Walker, 1998). It was only by explicitly allowing for spatial and stock structure, and by using tagging data for estimation purposes in the third type of model for the 1999 assessment, that uncertainty was substantially reduced. The third model, henceforth referred to as the spatially structured stock assessment model, estimated the pup production at the start of 1997 to be 12–18% of the 1927 level (Punt et al., 2000b).

Stock assessment incorporating movement rates and stock structure The 1999 assessment used data from three separate tagging programs. Tagged sharks were released during 1947–1956 (Olsen, 1954), 1973–1976 (Walker, 1989a), and 1990–1999 (Brown et al., 2000). Of 9,819 G. galeus tagged, 1,255 (or 13%) had been recaptured and reported by the end of 1999 (Brown et al., 2000). Data from these tagging programs have been used in various ways to assess movement dynamics. One of these methods involved simply plotting release and recapture positions on a map to provide a description of broad movement patterns (Olsen, 1954; Brown et al., 2000). Vector analysis has been applied to provide a quantitative basis for comparing differences in movement between sharks of different species, sex, size, and region (Brown et al., 2000; Walker et al., 2000). These approaches have helped develop alternative hypotheses of movement, but have been inadequate for determining rates of movement between eight separate regions, which were required in the age-based and spatially structured stock assessment model developed for the 1999 stock assessment. The present work considers the application of three models that explicitly model the movement of G. galeus in the southern Australian population. Two of these models – the movement simulation model (1º latitude  1º longitude cells) and the spatially structured stock assessment model (eight regions) – were used to undertake the 1999 stock assessment. The third model – the integrated tag model (three regions) – was developed more recently.

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This third model is similar to one developed to provide an experimental design for tagging M. antarcticus and G. galeus off southern Australia during 1993–1996 (Xiao, 1996) and a generalized simpler method applied in other fisheries (Hilborn, 1990). It will be used in future assessments for quantifying broad-scale movement rates that can help further develop movement hypotheses. The spatially structured stock assessment model includes parameters that determine the probability of movement among eight regions by month for each of 21 age classes. It is clearly impossible to estimate each of these parameters using the available data. Instead, the movement simulation model was used to represent alternative hypotheses of movement by tuning it through trial and error. Initial estimates of movement were produced by essentially setting to zero the monthly movement probabilities for combinations of regions between which movement must be zero. These initial estimates were then modified using 36 parameters in the assessment model to better fit the tagging data (Punt et al., 2000b).

Movement simulation model Two alternative movement hypotheses were considered for conceptual purposes when developing the age-based and spatially structured stock assessment model. However, the available data fit the assessment model best when a mix of the two hypotheses was adopted. The two hypotheses can be stated as follows: (1) a single panmictic population with components at different life-history stages occupying separate localities within the range of its distribution and (2) spatially discrete subpopulations with no or very limited interbreeding. The first hypothesis – the single-stock hypothesis – is consistent with the breeding patterns and large-scale movements described for this species (Olsen, 1954) and with most data collected subsequently (Brown et al., 2000). The second hypothesis – the multiplesubstock hypothesis – was assumed when the stocks were assessed as spatially separate stocks in eight different regions as part of an earlier assessment (Prince, 1991). This second hypothesis is consistent with different trends in different regions and the apparent present lack of animals off the east coast of Australia. The intermediate hypothesis adopted for the 1999 assessment requires separate breeding substocks, but mixing of the substocks at other life-history stages (Punt et al., 2000b). This hypothesis has elements of both conceptual hypotheses and is referred to as a “mixing multiple-substock hypothesis,” which might be explained by concepts such as philopatry effected through “natal homing” (Hueter, 1998; Hueter et al., 2005). If each pregnant shark returns to its own place of birth for parturition, then there would effectively be a separate substock associated with each major nursery area. Such behavior could maintain functionally separate substocks even if breeding occurred between animals from different substocks. The movement simulation model operates on a daily time-step and considers movement of individuals within each age class in the whole population or a particular subpopulation between contiguous cells 1º of latitude by 1º of longitude in size. A matrix of movement probabilities was selected to represent a mix of large-scale pupping migrations, feeding migrations, and random movement. The movement is displayed on a map of southern Australia by a computer program, and alternative hypotheses can be simulated by

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specifying values for a small number of behavior-related parameters (e.g., the probability of randomly leaving a cell). Net movement in one direction is achieved by setting the probability of moving in one direction greater than that in the opposite direction (Taylor, 1997). The results from this model are then aggregated to monthly and regional resolution and used as initial values for estimating movement rates in the spatially structured stock assessment model.

Spatially structured stock assessment model The spatial structure of the fishery was made explicit for the 1999 assessment by dividing the fishery into eight regions (Fig. 32.1). In addition, the model allowed for multiple stocks to evaluate a range of alternative hypotheses for stock structure and movement. The model includes demographic parameters to represent the growth of sharks and the pupping and recruitment processes, as well as multiple gears (gill nets of various mesh size and hooks) with their selectivity parameters (Punt et al., 2000b). For the purpose of this model, a stock is defined as “a group of animals that have the same pupping grounds and movement patterns.” The model is fitted simultaneously to data disaggregated into the eight regions, and the assessment is based on the assumption that two stocks of G. galeus occur off southern Australia, which are distinct from the stock in New Zealand. A two-stock model was found to fit the data better than a singlestock model that allows for movement, but the data cannot support estimation of parameters for models based on more than two stocks. Movement patterns differ between the two stocks. The probability of moving among regions is assumed to depend on month and age to represent the patterns observed from tagging data. Parturition is assumed to occur only in the eastern region of the fishery. The model allows sharks from New Zealand to move to Australia, where they can be caught. Only animals aged 6–12 years (evidenced by tag returns) are assumed to move from New Zealand to Australia. It is also assumed that there is a 50% probability that a New Zealand G. galeus in Australia returns to New Zealand each year. Furthermore, fishing in either country is assumed to have negligible impact on the population in New Zealand because few of these sharks are present in Australia, and the level of fishing mortality in New Zealand is much lower than that in Australia. The basis of this assumption is a 5.2% tag recovery rate during 1985–1997 for New Zealand (Hurst et al., 1999) compared with a 20.1% recovery rate during 1990–1999 for Australia (Brown et al., 2000). For this reason, movement of Australian animals to New Zealand is ignored. A range of 0–15% is examined for the percentage of animals aged 6–12 years in Australia (in the prefishing condition) that originated in New Zealand.

Movement estimation within an integrated tag model The integrated tag model is designed for estimating movement, mortality, and growthrate parameters from tag release–recapture data (see Appendix). For the present analyses, the model was used to estimate movement and mortality using data collected during 1990–1999. As part of the movement analysis, the effects of sex and total length (TL) were tested. The model accounts for the growth of tagged sharks at liberty and the selectivity

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characteristics of 6-, 6½-, and 7-inch-mesh gill nets and longlines used in the fishery. Annual nominal fishing effort (calendar year) for each of these four fishing gears was applied in the model for the 10-year period of the analysis. Three separate zones, rather than the eight regions adopted for the spatially structured stock assessment model because of data limitations, were adopted for the analysis: Western Australia/South Australia (WA/SA), Bass Strait (BS), and Tasmania (Tas). The WA/SA region includes all waters adjacent to South Australia plus a small region off the southern coast of Western Australia where G. galeus occurs. This small region (127–129ºE) extends 2º of longitude west of the WA/SA border. The BS zone is demarcated from the SA zone by the South Australia–Victoria border and from the Tas zone by latitude 41ºS (close to the north coast of Tasmania). The Tas zone includes water off Tasmania south of latitude 41ºS (Fig. 32.2). Estimates of annual movement rates among the three zones were made for separate length classes chosen to approximate broad stages of maturity. The four categories chosen were: males and females combined, 650–1,199 mm TL; males and females combined, 1,200–1,399 mm TL; males 1,400 mm TL; and females 1,400 mm TL. These categories are referred to as juveniles, subadults, mature males, and mature females, respectively. From one time-step to the next (1 year in the present analysis) in the model, the number of sharks within each category can change as the sharks grow. Not all length classes were well represented in every zone because there is a lack of small sharks in WA/ SA and large sharks in BS. Several types of tag were used, which are broadly categorized as dart tags (23% of the total) and rototags (77%) (Table 32.2). Most of the dart tags were nylon-headed and were either inserted into the dorsal muscle tissue (13%) or anchored by the cartilage at the base of the first dorsal fin (8%). Some of the tags in this category were steel-headed dart tags and nylon T-tags (2%). Most of the tags in the rototag category were medium-sized rototags (18%) and large-sized rototags ( jumbo tags) (45%), which were attached at the lower anterior region of the first dorsal fin. Also included in the rototag category were imitation archival tags, used for testing the attachment procedures of archival tags, and archival tags. These tags were either pinned to the first dorsal fin and secured with a “jumbo tag” or inserted into the coelomic cavity (14%). Twelve percent of the tagged sharks were double-tagged with a dart tag and a rototag. For analysis, a tagged shark returned with two tags was treated as having been tagged with a dart tag, because the tag-shedding rate was much higher for dart tags than for rototags.

Table 32.2 Number of tagged sharks (male and female) by tag type for each release region in the estimation.* Type of tag

WA/SA

BS

Tas

Total

Rototag Dart tag Total

636 189 825

359 86 445

582 202 784

1,577 477 2,054

Includes only sharks 650 mm TL when tagged and released during 1990–1998. WA/SA: Western Australia (127–129ºE)/South Australia; BS: Bass Strait; Tas: Tasmania.

*

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The analysis used 2,054 tagged and released sharks, of which 434 (21%) were recaptured and reported (Table 32.3); any sharks 650 mm TL at release were excluded. The “tag reduction rate” ( joint natural mortality rate and tag-shedding rate) was estimated for the dart tags and rototags separately, because double-tag experiments demonstrated that tag-shedding rate varied markedly between these types of tag (Xiao et al., 1999). Six movement parameters (two directions for each of three zones) were estimated for each of the four sex–TL categories. Three additional movement parameters for each of the sex–TL categories, representing the sharks that did not change zones, were simply calculated from the other six movement parameters. Three catchability parameters (one for each zone), a “tag survival ratio” (proportion of tags surviving release and recapture processes) assumed to be independent of zone and tag type, and two “tag reduction rate” parameters (one for each category of tag type) were estimated. This gave a total of 30 parameters to estimate and 12 parameters that were calculated from the estimated 30 parameters (Table 32.4). Juveniles tend to move out of Tas: 42% annually moved from Tas to WA/SA and 20% annually moved from Tas to BS, with no returns to Tas from either of the other two zones. However, there was a strong trend for the larger sharks to move to Tas, with a tendency to remain in Tas: 72% of subadults, 80% of mature males, and 52% of mature females remained in Tas each year. There was also a strong trend for mature females to move to SA (Table 32.4 and Fig. 32.3). Parameter estimates for “catchability,” the “tag survival ratio,” and the three “tag reduction rates” were found to be correlated with each other, but only weakly correlated with the movement rate parameters (Table 32.5). Gill-net catchability estimates varied markedly

Table 32.3 Distribution of recaptured and unrecaptured tagged sharks by region of release and recapture in the estimation.* Sex

Recapture region or unrecaptured

Number of recaptured and unrecaptured sharks by release region WA/SA

BS

Tas

Total

Male

WA/SA BS Tas Unrecaptured Total

51 11 6 240 308

10 46 7 225 288

18 20 32 321 391

79 77 45 786 987

Female

WA/SA BS Tas Unrecaptured Total

84 14 7 412 517

15 27 5 110 157

37 25 19 312 393

136 66 31 834 1,067

Total

WA/SA BS Tas Unrecaptured Total

135 25 13 652 825

25 73 12 335 445

55 45 51 633 784

215 143 76 1,620 2,054

*Includes sharks recaptured and reported, and sharks unrecaptured, during 1990–1999. WA/SA: Western Australia (127–129ºE)/South Australia; BS: Bass Strait; Tas: Tasmania.

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Table 32.4 Estimates of annual movement rates and instantaneous mortality rates.* Sex/size

Estimated parameter

Recapture region

Annual movement rate between regions, prr (year1)

WA/SA

Subadults Annual 1,200–1,399 mm movement TL rate between regions, prr (year1)

WA/SA

Male adults 1,400 mm TL

Annual movement rate between regions, prr (year1)

WA/SA

Annual movement rate between regions, prr (year1)

WA/SA

Juvenile 650–1,199 mm TL

Female adults 1,400 mm TL

Total

Catchability, qr (104 year1)

BS Tas

BS Tas

BS Tas

BS Tas

Parameter estimate (with 90% probability interval) for each release region WA/SA

BS

Tas

0.975 (0.917, 0.997) 0.025 (0.003, 0.067) 0.000 (0.000, 0.002)

0.162 (0.036, 0.301) 0.838 (0.677, 0.939) 0.000 (0.000, 0.010)

0.414 (0.270, 0.588) 0.202 (0.115, 0.332) 0.383 (0.208, 0.565)

0.736 (0.573, 0.843) 0.089 (0.041, 0.159) 0.175 (0.056, 0.342)

0.210 (0.034, 0.502) 0.318 (0.119, 0.594) 0.472 (0.131, 0.743)

0.179 (0.107, 0.287) 0.098 (0.049, 0.177) 0.723 (0.607, 0.799)

0.812 (0.475, 0.983) 0.105 (0.002, 0.469) 0.083 (0.005, 0.501)

0.244 (0.066, 0.715) 0.510 (0.115, 0.751) 0.246 (0.053, 0.771)

0.068 (0.008, 0.237) 0.124 (0.029, 0.389) 0.808 (0.460, 0.931)

0.706 (0.515, 0.865) 0.045 (0.006, 0.135) 0.249 (0.092, 0.402)

0.036 (0.005, 0.458) 0.522 (0.154, 0.917) 0.441 (0.066, 0.838)

0.433 (0.216, 0.862) 0.047 (0.008, 0.150) 0.520 (0.087, 0.740)

0.150 (0.089, 0.236)

0.547 (0.295, 0.885)

1.667 (0.830, 3.326)

Combined

Tag recovery ratio, ξ

0.393 (0.277, 0.609)

Rototag reduction rate, ζ1 (year1)

0.170 (0.030, 0.311)

Dart tag reduction rate, ζ2 (year1)

0.411 (0.200, 0.607)

* Gill-net selectivity parameters of θ1  188.0 and θ2  55,920, and Francis growth length-increment parameters of gλ  126 and gµ  70 mm/year for males, and gλ  133 and gµ  44 mm/year for females, where λ  800 mm TL and µ  1,200 mm TL were provided exogenously.

between SA (0.150  104 year1), BS (0.547  104 year1), and Tas (1.667  104 year1) (Table 32.4). The catchability of a unit of longline fishing effort (1,000 hook-lifts) was assumed to equal the catchability of a unit of gill-net fishing effort (1,000 meterlifts). Independent estimates of hook catchability relative to gill-net catchability are ⬃1 (Primary Industries Research Victoria, unpublished data). This assumption avoided the need to estimate three additional catchability parameters for longline fishing effort (one

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Male and female juveniles 650–1,999 mm 2%

Remaining: 98% WA/SA

Remaining: 84% BS

42% 16%

20% Tas 0% 0% Remaining: 38%

Male and female subadults 1,200–1,399 mm Remaining: 74%

9%

BS

18% 21%

WA/SA

Remaining: 32%

10% Tas 17% 47% Remaining: 72%

Males

1,400 mm 11%

Remaining: 81%

BS

7% 24%

WA/SA

Remaining: 51%

13% Tas 8% 25% Remaining: 80%

Females

1,400 mm 4%

Remaining: 71% WA/SA

43% 4%

Remaining: 52% BS 5%

Tas 25% 44% Remaining: 52% Fig. 32.3 Annual movement rates between three zones. BS: Bass Strait; Tas: Tasmania; WA/SA: Western Australia (127–129ºE) and South Australia combined.

Table 32.5 Correlation coefficients between parameter estimates.*

*Four sex-length-class categories for movement rates are males  1,400 mm TL (adult males) and females  1,400 mm TL (adult females), males and females combined 1,200–1,399 mm TL (subadults), and males and females combined 650–1,199 mm TL (juveniles). The symbol  denotes the “tag survival ratio,” 1 the “rototag reduction rate,” and 2 the “dart tag reduction rate.” The symbol prr denotes the probability of movement from region r to region r, where 1 is WA/SA, 2 is BS, and 3 is Tas [WA/SA, Western Australia (127–129°E)–South Australia; BS, Bass Strait. Tas, Tasmania]. The symbol qr is catchability in region r.

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for each zone). The assumption can be justified on low longline fishing effort (Walker, 1999b) and on the small number of tags recaptured by longline. This makes the analyses insensitive to the catchability values used. If estimates of these parameters were made from the present analysis, the bounds of uncertainty would be very high. The differences in the catchability values among the zones are surprisingly large. In the present study, each of these values is a measure of the relative proportion of the population of animals in a zone encountering (not captured by) the fishing gear associated with one unit of fishing effort. Several factors are probably contributing to the higher catchability value in Tas than in WA/SA and BS. In Tas, the catch is mainly G. galeus, whereas the catch of M. antarcticus is negligible; this suggests that most of the fishing effort is targeted at G. galeus. In contrast, most of the effort in BS and much of the effort in WA/SA is targeted at M. antarcticus. In Tas, much of the effort is applied seasonally when the animals are predictably aggregated in a relatively small area; the continental shelf area in Tas is much smaller than in either WA/SA or BS. Greater targeting of G. galeus in WA/SA than in BS would contribute to a higher catchability value for WA/SA than for BS. However, the effect of targeting is offset by the spatially much larger area fished in WA/SA than in BS. In BS, the catch is taken in a zone where the largest component of the G. galeus population 650 mm TL occurs; this is where most of the juveniles and a major portion of the subadults occur. Although the catch mass from WA/SA is only marginally higher than the catch mass from BS (Walker, 1999b), many more animals are landed from BS than from WA/SA. This is because the mean mass of animals captured in BS is about half the mass of those taken in WA/SA (Walker et al., 2003). The estimates of tag reduction rate are 0.170 year1 for rototags and 0.411 year1 for dart tags (Table 32.4). Given that the tag reduction rate equals the sum of natural mortality rate and tag-shedding rate (see Appendix), an available value for natural mortality rate would provide an indication of tag-shedding rate. A value of 0.100 year1 for the natural mortality rate is commonly adopted for stock assessment of G. galeus in southern Australia (Punt and Walker, 1998; Punt et al., 2000b); this value is similar to estimates from an earlier tagging program (Grant et al., 1979). Use of this natural mortality rate in the present analysis provides estimates of tag-shedding rates similar to those determined independently from double-tag experiments (Xiao et al., 1999). Subtracting 0.100 year1 for natural mortality from the tag reduction rate of 0.170 year1 suggests a tag-shedding rate of 0.070 year1 (7% annually) for rototags (Table 32.6). This agrees well with the independent estimate for tag-shedding rate of 0.088 year1 (8% annually) for rototags (Xiao et al., 1999). Subtracting the same for natural mortality from the tag reduction rate of 0.411 year1 suggests a tag-shedding rate of 0.311 year1 (27% annually) for dart tags. This does not agree quite so well with the independent estimate of 0.425 year1 (35% annually) for dart tags (Xiao et al., 1999); the reasons for this are unclear. An estimate of the “tag–release survival ratio” (tag survival from “initial capture and tag-induced mortality” and “initial tag shedding”) can be obtained by comparing the estimate of the “tag survival ratio” (0.393) with an independent estimate of tag reporting ratio (⬃0.70) (Brown and Walker, 1999). This implies a “tag–release survival ratio” of roughly 56%, which means 44% of the tags were lost through “initial capture and tag-induced mortality” and “initial tag shedding.” This estimate is rather uncertain, as the 0.70 value is poorly defined and the 0.393 is not particularly precise. However, it does suggest strongly

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Table 32.6 Comparison of estimated tag-shedding rates. Type of tag

Rototag Dart tag

Number taggeda

1,616 438

Rate (year1) Tag reductionb

Natural mortalityc

Differenced

Tag sheddinge

0.170 0.411

0.100 0.100

0.070 0.311

0.088 0.425

Number of tagged sharks released 650 mm TL. Tag reduction rate estimates from Table 32.3. c Assumed natural mortality rate. d Tag reduction rate minus natural mortality rate as an approximation for tag-shedding rate. e Values of tag-shedding rate from Xiao et al. (1999). a

b

that ignoring “initial capture and tag-induced mortality” and “initial tag shedding” when using tagging data in fisheries stock assessments is inappropriate. In general, the results from the integrated tag model indicate that large females tend to move to WA/SA, which is consistent with the trends for the commercial fishers to catch more females than males in this zone (Walker et al., 2003). This is also consistent with the original theory of movement. The results from this estimator indicate that large males move to Tas, which is consistent with the trends for the commercial fishers to catch more males than females in Tas (Primary Industries Research Victoria, unpublished data). This trend, however, is not consistent with the original theory of movement. This more recently discovered pattern of movement and distribution for adult males is more consistent with the distribution patterns of G. galeus on the eastern coast of South America and on the western coast of North America. In both of these populations, the females aggregate in the warmer waters and the males in the cooler waters during the winter months (Walker, 1999a). The results from the integrated tag model are consistent with the “single panmictic population” hypothesis and with the “mixing multiple-substock hypothesis,” but are inconsistent with the “spatially discrete substocks hypothesis.” These results indicate the need to represent the movement pattern of the mature males differently from the movement pattern of the mature females in both the movement simulation model and the spatially structured stock assessment model. This might alter the results slightly from the 1999 assessment, which assumed that males and females have identical movement patterns. The two-stock movement patterns produced by fitting the tag data to the spatially structured stock assessment model resemble the separate male and female patterns. So far, the integrated tag model has been used only for estimating annual rates of movement between zones, but it needs to be developed further to allow for seasonal effects in movement and fishing effort.

Conclusions Various modeling approaches have improved our understanding of the movement patterns and stock structure of G. galeus off southern Australia, and further modeling with available data sets is likely to provide more insights. Large-scale movements of tagged

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animals and structuring by size, age, and breeding condition across southern Australia tend not to support the presence of spatially discrete substocks. However, the presence of reproductively distinct substocks that mix during parts of their life cycle, or of behaviorally discrete substocks, remains uncertain, and improved understanding will require the application of additional stock discrimination techniques, such as genetic and parasite methods. Genetic comparison of samples of neonates from widely separated nursery areas would be a valuable first step, though it will be essential to collect the animals before they are large enough to leave the nursery areas and mix with animals from other nursery areas. Notwithstanding our incomplete knowledge, the recent incorporation of tag data directly into the assessment, using spatially structured models to embrace alternative movement hypotheses, has turned highly uncertain assessments into ones in which we can have greater confidence.

Appendix: movement estimation within an integrated tag model Model parameters Rates of movement among regions of the fishery and rates of mortality were estimated by maximum likelihood using tag release–recapture data (length and date of release, and date of recapture) and fishing effort data (by gear type and region) (Dow, 1989, 1992; Dow and Kirkwood, 1989; Dow and Walker, 1989). The values for the parameters of the model that maximize the posterior density function along with 90% Bayesian probability intervals and the parameter estimate covariances were obtained using the Markov Chain Monte Carlo method as implemented in the AD Model Builder package (Fournier, 1996). Although the parameters of the growth function can also be estimated within this framework, these parameters were instead assumed known based on auxiliary information (Dow and Walker, 1989; Dow, 1992). The selectivity patterns for each gear type were also assumed to be known exactly from gill-net selectivity experiments (Kirkwood and Walker, 1986). The model did not include Bayesian prior distributions for any parameters. For the purpose of the model, the term “rate of movement” is defined as the proportion of animals leaving one region to move to another region within a specified period (1 year in the present study). Each tag (whether recaptured or not) makes a separate contribution to the likelihood function, and the likelihood function is the product over all tagged animals of the likelihood contribution for each animal. The parameters of the model determined by maximizing the likelihood function are the annual movement rates (“movement probabilities”) each way between each pair of separate regions, the catchability of the fishing gear in each region, the “tag reduction rate” for each tag-type z (ζz), and the “tag survival ratio” (ξ). Each “tag reduction rate” includes the two confounded additional factors of “natural mortality rate,” M, and “tag-shedding rate,”ηz, such that ζz  M ηz. The “tag survival ratio” is the number of tags recaptured and reported expressed as a proportion of the expected number of tags recaptured had there been no tag loss through the initial tag release process and subsequent tag recapture process. This parameter accounts for several confounded factors that can be grouped as factors associated with

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the initial release of tagged animals and those associated with the subsequent recapture of tagged animals. These two groups of factors are referred to as the “tag–release survival ratio” (ξ1) and “tag–recapture survival ratio” (ξ2), respectively, and can be logically grouped in the equation ξ  ξ1ξ2. The “tag–release survival ratio” accounts for tag survival from “initial capture and tag-induced mortality” and “initial tag shedding.” The “tag–recapture survival ratio” accounts for “nonreporting of tags by fishers” and “nonsighting of tags by fishers.” The first of these is the failure to report a recovered tag, and the second includes the factors of “predation mortality during recapture,” “dropout mortality,” and dislodgment of tags occurring after recapture of a tagged animal but before retrieval of the fishing gear, and oversight of tags during handling and processing of animals aboard a vessel after retrieval of the fishing gear. The expressions and nomenclature adopted in the likelihood function are defined by several equations. In the following, the dependence of model quantities and likelihood contributions on the time at release (τ0) has been suppressed for ease of presentation.

Likelihood function The contribution to the likelihood function by a shark that was recaptured during period τf in region r is given by the equation L1  πτ

f

,r , z

cτ

f

,r , z

where L1 is the product of the probability that the shark tagged with tag-type z was in region r during period τf (πτ ,r,z) and the probability that it was recaptured and reported f in region r during period τf given that it was present (cτ ,r,z). The contribution to the likelif hood function by a shark that was not recaptured is given by the equation R

L2  1  ∑

T

∑

r1 τ τ 0

πτ ,r ,z cτ ,r ,z

where L2 is 1 less the probability that the shark was recaptured and reported in any of R regions until the period T, the final period under investigation, and τ0 is the period during which the shark was tagged and released.

Movement and survival Initially, πτ

0 ,r ,z

 ξ1 pr ′ r (l )∆τ eζ z ∆τ

where ∆τ is the fraction of the period from the time at release to the end of the release period and prr (l ) is the probability of movement from region r to region r of R regions

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for an animal of length l. To allow tagged sharks to be randomly mixed with the rest of the population, those recaptured during period τ0 are rejected from the analysis. For animals not recaptured during τ0, the fishing mortality during τ0 is assumed to be zero. The probability of arrival in region r at the start of period τ can then be calculated recursively by the equation πτ , r , z 

R

∑ πτ1,r ′,z sτ1,r ′z (l ) pr ′r (l )

r ′1

where “survival” during period τ in region r for animals of length l tagged with tag-type z, sτ,r,z (l), is given by the equation sτ ,r ,z (l ) = e

⎡⎢ ζ z Fτ ,r ( l ) ⎤⎥ ⎦ ⎣

Mortality The probability of a shark of length l tagged with tag-type z in region r during period τ being recaptured and reported is given by the equation cτ ,r ,z (l ) 

ξ2 Fτ ,r (l ){1  e[ζ z Fτ ,r ( l )]} ζ z Fτ ,r (l )

where Fτ,r(l ) is the fishing mortality rate for an animal of length l during period τ in region r. It can now be seen that πτ ,r,z, and hence each πτ,r,z, is proportional to ξ1 and that cτ,r,z 0 is proportional to ξ2. In the likelihood functions L1 and L2, πτ,r,zcτ,r,z and, hence, ξ1ξ2 only appear as a product. It is therefore only necessary to estimate ξ, the “tag survival ratio.” There is now evidence from fishery modeling that natural mortality must be much higher in newborn and small sharks than in larger sharks (e.g., M. antarcticus: Walker, 1994; Pribac et al., 2005; G. galeus: Punt and Walker, 1998; Punt et al., 2000b). Hence, in the present study, to accommodate the constant M assumption implicit in the equation used to define Fτ,r (l ), only animals 650 mm TL when tagged and released are included in the analyses. Fishing mortality is assumed to be separable into length and year effects, and includes contributions from each of the gear types used in the fishery as in equation J

Fτ ,r (l )  qn,r ∑ f j ,τ ,r µ j (l ) qh,r f h,τ ,r µh (l ) j1

where qn,r is the catchability coefficient for gill nets in region r (for J mesh sizes of gill net), qh,r is the catchability coefficient for hooks in region r, fj,τ,r is the fishing effort for gill-net mesh size j in region r during period τ, fh,τ,r is the fishing effort for hooks in region r during period τ, and µj(l ) is the selectivity for gill nets of mesh size j on animals of length l. Selectivity for hooks can be assumed to be uniform (i.e., µh(l )  1).

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Gill-net selectivity (Kirkwood and Walker, 1986) is given by equation µ j (l )  (l / α j β j )α j e ( α j l / β j ) where αj and βj are parameters related to mesh size, mj, and the length of fish, l, where it is assumed that the length of the shark at maximum selectivity for gill net j is proportional to the mesh size. Hence αjβj  θ1mj where θ1 is the constant of proportionality and the variance is constant θ2 for all mesh sizes. For positive βj, these assumptions lead to the quadratic equation β j  0.5 ⎡⎢ θ1m j  [(θ12 m 2j 4θ2 )0.5 ]⎤⎥ ⎣ ⎦

Growth The predicted length of a fish l at time ∆t after its initial length of l0 when tagged and released is given by the equation ⎡ λg  γ g ⎤ ⎪⎧⎪ ⎡ gλ  g γ λ γ l  l0 ⎢⎢  l0 ⎥⎥ ⎪⎨1  ⎢⎢1

λγ ⎢⎣ gλ  g γ ⎥⎦ ⎪⎪ ⎢⎣ ⎪⎩

⎤ ∆t ⎪⎫⎪ ⎥ ⎪ ⎥ ⎬⎪ ⎥⎦ ⎪ ⎪⎭

where gλ and gγ are the mean annual growth increments of sharks (males and females separately in the present study) of arbitrary lengths λ and γ, respectively, where λ and γ are chosen to represent the range of the lengths observed in tagged or recaptured sharks (Francis, 1988; Dow and Walker, 1989; Dow, 1992). Length is used in the calculations of gear selectivity and in the assignment of the appropriate movement rate for the length class of the animal during a given period.

Acknowledgments The availability of the tag data used in the present analyses can be attributed to the active participation and cooperation of many people in Australian Commonwealth and State fisheries research and management agencies, and in commercial and recreational fishing bodies. We thank all of those many individual professional and recreational fishers who tagged sharks, captured sharks for tagging, or returned tags. Nik Dow, formerly of Primary Industries Research Victoria, is acknowledged for his early work developing the integrated tag model and a FORTRAN computer program for its implementation.

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Recent tag data were collected mostly as part of two projects undertaken over 6 years, funded by the Fisheries Research and Development Corporation (FRDC). The first project was the Southern Shark Tagging Project (FRDC 93/066), a 3-year project during 1994–1996 to design, implement the tagging of sharks, and manage tag recaptures. The second was the Southern Shark Tag Database Project (FRDC 96/162), a 3-year project during 1997–1999 to manage tag recapture data and allow time for sufficient tag recaptures. Sharks were also tagged opportunistically as part of the project Investigation of School Shark Nursery Areas in South Eastern Australia (FRDC 93/061).

References Brown, L. P. and Walker, T. I. (1999) Tag reporting rates for gummy and school shark estimated from catch and from tags per unit catch. In: Southern Shark Tag Database Project (eds. T. I. Walker, B. L. Taylor and L. P. Brown). Final Report to Fisheries Research and Development Corporation, Project No. 96/162. Marine and Freshwater Resources Institute, Queenscliff, Victoria, Australia, pp. 67–80. Brown, L. P., Bridge, N. F. and Walker, T. I. (2000) Summary of Tag Releases and Recaptures in the Southern Shark Fishery. Report No. 18. Marine and Freshwater Resources Institute, Queenscliff, Victoria, Australia, 61 pp. Casey, J. G. (1985) Transatlantic migrations of the blue shark: A case history of cooperative tagging. In: World Angling Resources and Challenges: Proceedings of the First World Angling Conference (ed. R. H. Stroud). International Game Fish Association, Fort Lauderdale, FL, pp. 253–268. Coleman, N. and Mobley, M. (1984) Diets of commercially exploited fish from Bass Strait and adjacent Victorian waters, south-eastern Australia. Australian Journal of Marine and Freshwater Research 35, 549–560. Compagno, L. J. V. (1984) FAO Species Catalogue. Vol. 4. Sharks of the World: An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 2. Carcharhiniformes. FAO Fisheries Synopsis No. 125. FAO, Rome, Italy, pp. 251–655. Dow, N. G. (1989) Quantification of rates of movement from tagging data. In: Southern Shark Assessment Project – Final FIRTA Report: March 1989 (eds. T. I. Walker et al.). Marine and Freshwater Resources Institute, Queenscliff, Victoria, Australia. Dow, N. G. (1992) Growth parameter estimation from tagging and ageing data. In: The Measurement of Age and Growth in Fish and Shellfish (ed. D. A. Hancock). Bureau of Rural Resources, Canberra, Australian Capital Territory, Australia, pp. 185–192. Dow, N. G. and Kirkwood, G. P. (1989) Mortality and length increment estimation from tagging data. In: Southern Shark Assessment Project – Final FIRTA Report: March 1989 (eds. T. I. Walker et al.). Marine and Freshwater Resources Institute, Queenscliff, Victoria, Australia. Dow, N. G. and Walker, T. I. (1989) Growth parameter estimation from tagging and ageing data in a length-selective fishery. In: Southern Shark Assessment Project – Final FIRTA Report: March 1989 (eds. T. I. Walker et al.). Marine and Freshwater Resources Institute, Queenscliff, Victoria, Australia. Ellis, J. R., Pawson, M. G. and Shackley, S. E. (1996) The comparative feeding ecology of six species of shark and four species of ray (Elasmobranchii) in the north-east Atlantic. Journal of the Marine Biological Association of the United Kingdom 76, 80–106. Ford, E. (1921) A contribution to our knowledge of the life histories of the dogfishes landed at Plymouth. Journal of the Marine Biological Association of the United Kingdom 12, 468–505. Fournier, D. (1996) An Introduction to AD Model Builder for Use in Nonlinear Modeling and Statistics. Otter Research Ltd., Nanaimo, British Columbia, Canada.

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Francis, R. I. C. C. (1988) Maximum likelihood estimation of growth and growth variability from tagging data. New Zealand Journal of Marine and Freshwater Research 22, 42–51. Freer, D. W. L. (1992) The Commercial Fishery for Sharks in the South-Western Cape, with an Analysis of the Biology of the Two Principal Target Species, Callorhynchus capensis Dumeril and Galeorhinus galeus Linnaeus. M.Sc. thesis, University of Cape Town, Cape Town, South Africa. Grant, C. J., Sandland, R. L. and Olsen, A. M. (1979) Estimation of growth, mortality and yield per recruit of the Australian school sharks, Galeorhinus australis (Macleay), from tag recoveries. Australian Journal of Marine and Freshwater Research 30, 625–637. Gubanov, Y. P. and Grigor’yev, V. N. (1995) Observations on the distribution and biology of the blue shark Prionace glauca (Carcharhinidae) of the Indian Ocean. Voprosy Ikhtiologii 15, 43–50 (in Russian). Hanchet, S. M. (1986) The Distribution and Abundance, Reproduction, Growth, and Life History Characteristics of the Spiny Dogfish, Squalus acanthias (Linnaeus), in New Zealand. Ph.D. thesis, University of Otago, South Island, New Zealand. Herald, E. S. and Ripley, W. E. (1951) The relative abundance of sharks and bat stingrays in San Francisco Bay. California Fish and Game 37, 315–329. Hilborn, R. (1990) Determination of fish movement patterns from tag recoveries using maximum likelihood estimators. Canadian Journal of Fisheries and Aquatic Sciences 47, 635–643. Hisaw, F. L. and Albert, A. (1947) Observations on the reproduction of the spiny dogfish, Squalus acanthias. The Biological Bulletin (Marine Biology Laboratory, Woods Hole) 92, 187–199. Holden, M. J. and Harrod, R. G. (1979) The migrations of tope, Galeorhinus galeus (L.), in the eastern North Atlantic as determined by tagging. Journal du Conseil International pour l’Exploration de la Mer 38, 314–317. Hueter, R. E. (1998) Philopatry, natal homing and localised stock depletion in sharks. Shark News. The Newsletter of the IUCN Shark Specialist Group 12, 1–2. Hueter, R. E., Heupel, M. R., Heist, E. J. and Keeney, D. B. (2005) Evidence of philopatry in sharks and implications for the management of shark fisheries. Journal of Northwest Atlantic Fishery Science 35, 239–247. Hurst, R. J., Bagley, N. W., McGregor, G. A. and Francis, M. P. (1999) Movement of the New Zealand school shark, Galeorhinus galeus, from tag returns. New Zealand Journal of Marine and Freshwater Research 33, 29–48. Ketchen, K. S. (1986) The Spiny Dogfish (Squalus acanthias) in the Northeast Pacific and a History of Its Utilization. Publication No. 88. Department of Fisheries and Oceans, Ottawa, Quebec, Canada, 78 pp. Kirkwood, G. P. and Walker, T. I. (1986) Gill net mesh selectivities for gummy shark, Mustelus antarcticus Günther, taken in south-eastern Australian waters. Australian Journal of Marine and Freshwater Research 37, 689–697. Lucifora, L. O. (2003) Ecología y conservación de los grandes tiburones costeros de Bahía Anegarda, Provincia de Buenos Aires, Argentina. Ph.D. thesis, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina. Morato, T., Solà, E., Grós, M. P. and Menezes, G. (2003) Diets of thornback ray (Raja clavata) and tope shark (Galeorhinus galeus) in the bottom longline fishery of the Azores, northeastern Atlantic. Fishery Bulletin 101, 590–602. Nakano, H. (1994) Age, reproduction and migration of blue shark in the north Pacific Ocean. Bulletin of the National Research Institute of Far Seas Fisheries 31, 141–256. Nammack, M. F., Musick, J. A. and Colvocoresses, J. A. (1985) Life history of spiny dogfish off the northeastern United States. Transactions of the American Fisheries Society 114, 367–376.

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Olsen, A. M. (1954) The biology, migration, and growth rate of the school shark, Galeorhinus australis (Macleay) (Carcharhinidae) in south-eastern Australian waters. Australian Journal of Marine and Freshwater Research 5, 353–410. Peres, M. B. and Vooren, C. M. (1991) Sexual development, reproductive cycle, and fecundity of the school shark Galeorhinus galeus off southern Brazil. Fishery Bulletin 89, 655–667. Pribac, F., Punt, A. E., Walker, T. I. and Taylor, B. L. (2005) Using length, age and tagging data in a stock assessment of a length selective fishery for gummy shark (Mustelus antarcticus). Journal of Northwest Atlantic Fishery Science 35, 267–290. Prince, J. D. (1991) An Assessment of the South-Eastern Australian Shark Fishery. Biospherics Pty. Ltd., Perth, Western Australia, Australia. Punt, A. E. and Walker, T. I. (1998) Stock assessment and risk analysis for the school shark (Galeorhinus galeus) off southern Australia. Marine and Freshwater Research 49, 719–731. Punt, A. E., Walker, T. I., Taylor, B. L. and Pribac, F. (2000a) Standardization of catch and effort data in a spatially-structured shark fishery. Fisheries Research 45, 129–145. Punt, A. E., Pribac, F., Walker, T. I., Taylor, B. L. and Prince, J. D. (2000b) Stock assessment of school shark Galeorhinus galeus based on a spatially-explicit population dynamics model. Marine and Freshwater Research 51, 205–220. Ripley, W. E. and Bolomey, R. A. (1946) The relation between the biology of the soupfin shark to the liver yield of vitamin A. California Department of Fish and Game Fish Bulletin 64, 39–72. Saunders, M. W., McFarlane, G. A. and Smith, M. S. (1985) Results of Spiny Dogfish (Squalus acanthias) Tagging in British Columbia Waters during 1982 and 1983. Report No. 228. Fisheries and Oceans, Ottawa, Ontario, Canada. Stevens, J. D. (1990) Further results from a tagging study of pelagic sharks in the north-east Atlantic. Journal of the Marine Biological Association of the United Kingdom 70, 707–720. Stevens, J. D. and Wayte, S. E. (1999) A Review of Australia’s Pelagic Shark Resources. Fisheries Research and Development Corporation Project 98/107. CSIRO Marine Research, Hobart, Tasmania, Australia, 64 pp. Taylor, B. L. (1997) Movement modelling shell for school shark (Galeorhinus galeus) in the Australian southern shark fishery: A user’s guide to SSMOVE (Version 1). In: Southern Shark Tagging Project (eds. T. I. Walker, L. P. Brown and N. F. Bridge). Final Report to Fisheries Research and Development Corporation, Project No. 96/162. Marine and Freshwater Resources Institute, Queenscliff, Victoria, Australia, pp. 57–61. Walker, T. I. (1989a) Methods of tagging adopted in the southern shark fishery. In: Tagging – Solution or Problem? Australian Society for Fish Biology Workshop, Sydney (ed. D. A. Hancock). Australian Government Publishing Service, Canberra, Australian Capital Territory, Australia, pp. 105–108. Walker, T. I. (1989b) Stomach contents of gummy shark, Mustelus antarcticus Günther, and school shark, Galeorhinus galeus (Linnaeus), from south-eastern Australia. In: Southern Shark Assessment Project – Final FIRTA Report: March 1989 (eds. T. I. Walker et al.). Marine and Freshwater Resources Institute, Queenscliff, Victoria, Australia, pp. 1–24. Walker, T. I. (1994) Fishery model of gummy shark, Mustelus antarcticus, for Bass Strait. In: Resource Technology ’94 New Opportunities Best Practice (ed. I. Bishop). Centre for Geographic Information Systems and Modelling, University of Melbourne, Melbourne, Victoria, Australia, pp. 422–438. Walker, T. I. (1995) Stock Assessment of the School Shark, Galeorhinus galeus (Linnaeus), off Southern Australia by Applying a Delay-Difference Model. Marine and Freshwater Resources Institute, Queenscliff, Victoria, Australia, 28 pp. Walker, T. I. (1999a) Galeorhinus galeus fisheries of the world. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/2. FAO, Rome, Italy, pp. 728–773.

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Walker, T. I. (1999b) Southern Australian shark fishery management. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/2. FAO, Rome, Italy, pp. 480–514. Walker, T. I. (2005) Reproduction in fisheries science. In: Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids, and Chimaeras (ed. W. C. Hamlett). Science Publishers, Inc., Enfield, NH, pp. 81–127. Walker, T. I., Punt, A. E., Taylor, B. L. and Brown, L. P. (2000) Modelling school shark (Galeorhinus galeus) movement in the southern shark fishery. In: Fish Movement and Migration (eds. D. A. Hancock, D. C. Smith and J. D. Koehn). Australian Society for Fish Biology, Sydney, New South Wales, Australia, pp. 160–168. Walker, T. I., Hudson, R. J., Taylor, B. L. and Berrie, S. E. (2003) Southern Shark Monitoring Project 2003. Marine and Freshwater Resources Institute, Queenscliff, Victoria, Australia, 38 pp. Ward, R. D. and Gardner, M. G. (1997) Stock Structure and Species Identification of School and Gummy Sharks in Australasian Waters. Projects FRRF 93/11 and FRDC 93/64. CSIRO Marine Research, Hobart, Tasmania, Australia, 92 pp. West, G. J. and Stevens, J. D. (2001a) Archival tagging of school shark, Galeorhinus galeus, in Australia: Initial results. Environmental Biology of Fishes 60, 283–298. West, G. J., and Stevens, J. D. (2001b) The Use of Archival Tags for Studying the Movement and Swimming Behaviour of School Shark. Fisheries Research and Development Corporation Project 1996/128. CSIRO Marine Research, Hobart, Tasmania, Australia, 105 pp. Xiao, Y. (1995a) Integration of Standardization of Catch and Effort with Production Models for Stock Assessment. CSIRO Marine Research, Hobart, Tasmania, Australia, 29 pp. Xiao, Y. (1995b) Stock Assessment of the School Shark Galeorhinus galeus (Linnaeus) off Southern Australia by Schaefer Production Model. CSIRO Marine Research, Hobart, Tasmania, Australia, 55 pp. Xiao, Y. (1996) A framework for evaluating experimental designs for estimating rates of fish movement from tag recoveries. Canadian Journal of Fisheries and Aquatic Sciences 53, 1272–1280. Xiao, Y., Brown, L. P., Walker, T. I. and Punt, A. E. (1999) Estimation of instantaneous rates of tag shedding for school shark, Galeorhinus galeus, and gummy shark, Mustelus antarcticus, by conditional likelihood. Fishery Bulletin 97, 170–184.

Part V

Conservation and Management Outlook for Pelagic Sharks

Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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Introduction The final section of this volume focuses on efforts to conserve and manage the sharks of the open ocean. The current status of many populations of open sharks is unknown, and among those for which data are available, most are declining in abundance (Chapter 33). Despite some recent progress in data collection, assessment, and conservation measures, a great deal more management attention must be paid to these species if they are to reverse their declines or remain at healthy levels.

Data collection and assessment Over the past 15 years, growing concerns about the vulnerability and conservation status of sharks have provoked efforts to improve data collection. The International Commission for the Conservation of Atlantic Tunas was the first regional fishery management organization to request that its member nations report shark landings from the tuna and billfish fisheries that it oversees (Chapter 37). The Inter-American Tropical Tuna Commission, Indian Ocean Tuna Commission, Western and Central Pacific Fisheries Commission, and others have since done the same (Chapter 34). More countries are reporting shark landings than ever before, although many nations have no data on shark catches prior to the mid-1990s, and species-level reporting is still inadequate. Stock assessments have recently been conducted to determine the status of blue (Prionace glauca) and shortfin mako (Isurus oxyrinchus) sharks in the Atlantic (Chapter 37) and of porbeagle in the Northwest Atlantic (Lamna nasus; Chapter 35). Of these species, the blue shark population appears to be at a healthy level, shortfin mako appear to have declined, particularly in the North Atlantic, and the porbeagle population has collapsed. Evaluation of catch-rate data from fisheries shows apparent declines in abundance of pelagic (Alopias pelagicus), bigeye (A. superciliosus), and common (A. vulpinus) threshers, of white (Carcharodon carcharias), shortfin mako, silky (Carcharhinus falciformis), and oceanic whitetip (C. longimanus) sharks, and of some populations of blue sharks (Chapter 33). The salmon shark (L. ditropis) populations in both the Northeast and Northwest Pacific appear to be stable, as are some blue shark populations, and few data exist for pelagic stingrays (Pteroplatytrygon violacea). Because there are many shark populations for which no reliable data have been gathered, increased data collection efforts for pelagic elasmobranchs are necessary.

Shark fishery management Fisheries management for open ocean sharks has lagged behind that for coastal sharks, in part because their highly migratory nature demands regional and multinational cooperation (Chapter 34). A handful of the world’s 113 shark-fishing nations have implemented limited measures specifically for pelagic sharks, such as improved data collection, protected status (particularly for white sharks), and catch limits. Bans on shark finning also benefit pelagic sharks, which account for about one-third of the fins traded in Hong Kong. Overall, however, the taking of open ocean sharks remains largely unregulated.

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In 1999, the Food and Agriculture Organization of the United Nations adopted the International Plan of Action for the Conservation and Management of Sharks (IPOASharks), which called on all nations and regional fishery management organizations to develop and implement plans to improve the conservation status of sharks in their respective fisheries (Chapter 38). Progress toward implementation of the IPOA-Sharks has been slow: To date, only 6 nations have adopted a National Plan of Action, and 17 more have drafted but not yet approved a plan. A more positive development is that shark finning (the practice of cutting off just the fins and discarding the carcass) has been restricted by 17 nations, as well as the European Union, and an increasing number of regional fisheries organizations have prohibited finning in most international waters, although enforcement is often lacking. These actions to protect vulnerable shark populations from the wasteful practice of finning are a step in the right direction; however, caps on both directed and bycatch mortality will likely be necessary if fishing is to be sustainable without further threatening the status of these open ocean sharks.

New technologies The majority of the open ocean sharks killed in fishing operations are caught incidentally; therefore, reducing the bycatch of sharks is a key component of any management plan to conserve and rebuild pelagic shark populations. One approach is to close fishing grounds in times and areas where shark catches are high, particularly where reproductive females are present. Methods to modify fishing gears and practices also offer promise, such as using fabricated baits that are attractive to teleosts but not to sharks and reducing the soak times of longlines so that sharks that are caught will have a better chance of being released alive (Chapter 36). All of these approaches merit further study for use in high-seas fisheries where sharks are commonly caught but not retained.

Conclusion The story of the Northwest Atlantic porbeagle, which was overfished to the point of population collapse in the 1960s, and then – despite the availability of excellent fisheries data, a modern, sophisticated stock assessment, and a fishery management plan – collapsed again in the 1990s, demonstrates the critical need for precautionary management in fisheries taking open ocean sharks. The porbeagle’s history also emphasizes the importance of gathering data on shark fisheries, because the quality of the porbeagle data (and the assessment that these data supported) allowed fishery scientists to notice the 1990s collapse as it was occurring and to take steps to prevent further depletion. It must be noted, however, that no matter how good the available data and assessments, these species are probably not capable of sustaining high levels of fishing pressure. Thus, it is essential to develop sound fishery management plans that are precautionary and that account for the vulnerable life history of most sharks.

Chapter 33

Conservation Status of Pelagic Elasmobranchs Merry D. Camhi

Abstract Commercial fishing poses the greatest human-induced threat to open ocean elasmobranchs. Most fisheries fail to report species-specific landings and discards; this lack of data has precluded adequate population assessments, with the exception of that for the Northwest Atlantic porbeagle population. However, on the basis of fisheries trend data that are available, declines of 50–90% in catch rates over the past few decades have occurred, consistent with moderate to severe population declines for pelagic sharks in most waters. In addition, most pelagic elasmobranchs have been evaluated for inclusion on the IUCN Red List of Threatened Species: All three thresher species, white sharks, longfin and shortfin mako, porbeagle, and oceanic whitetip sharks are listed as globally Vulnerable, and blue sharks as Near Threatened. Most assessments to date suggest that pelagic sharks cannot sustain current fishing pressures and that precautionary fishery management measures to reduce mortality are needed immediately to help restore these populations. Key words: pelagic sharks, conservation, status, Red List, Threatened, Vulnerable, Endangered, population abundance.

Introduction It is now almost a cliché that, despite their fierce reputation, sharks are among the most vulnerable exploited species on the planet. This stems from the general tendency in chondrichthyan fishes to have low natural mortality, slow growth, late maturity, and low productivity. Because of these life-history constraints, which have been noted in almost every manuscript published on elasmobranch fisheries since 1990, sharks are more like large land mammals, cetaceans, and sea turtles than bony fishes in their capacity to sustain exploitation (Camhi et al., 1998; Musick, 1999). Unfortunately, numerous warnings from marine scientists, fishery managers, and conservationists have not yet resulted in well-managed shark fisheries or even attention in many places to the conservation needs of sharks (Camhi et al., 2008a). Pelagic sharks are particularly affected by fisheries because they are taken as directed catch and bycatch in longline and net fisheries Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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throughout the world, and are a major component of the international trade in shark fins (Clarke, 2003). Recent demographic analyses indicate that pelagic sharks fall within the middle range of shark reproductive productivities (Smith et al., 1998; Au et al., 2008) relative to the more productive small coastal species (e.g., smoothhounds, Triakidae) and the less productive large coastal sharks (e.g., dusky shark, Carcharhinus obscurus, Carcharhinidae). However, pelagic elasmobranchs span the productivity range from the bigeye thresher (Alopias superciliosus, Alopiidae), which is the least productive and ranks among the most vulnerable elasmobranchs, to the pelagic stingray (Pteroplatytrygon violacea, Dasyatidae), which is among the most productive, with the white (Carcharodon carcharias, Lamnidae), pelagic thresher (A. pelagicus, Alopiidae), silky (Carcharhinus falciformis, Carcharhinidae), salmon (Lamna ditropis, Lamnidae), porbeagle (L. nasus, Lamnidae), blue (Prionace glauca, Carcharhinidae), shortfin mako (Isurus oxyrinchus, Lamnidae), common thresher (A. vulpinus, Alopiidae), and oceanic whitetip (C. longimanus, Carcharhinidae) falling in between (Smith et al., 2008a). Despite their low to moderate productivities, it has been argued that pelagic sharks, especially blue sharks, are resilient to fishing pressure and are unlikely to become endangered. This notion derives from the perception that their widespread distribution and highly migratory nature preclude the possibility of population collapse or extinction through “seeding” and immigration (Smith et al., 1998). As a result, less conservation attention and management action have been directed toward pelagic sharks, especially when compared to coastal sharks. Notable declines, however, in a number of pelagic species, including blue sharks, belie this presumed resilience. In addition, the largely incidental nature of the catch and mortality of pelagic elasmobranchs makes it less likely that managers will detect depletions and other impacts of fishing. In addition, most pelagic sharks are apex predators within their open ocean habitat. The ecological impact of largescale removals of top oceanic predators is poorly understood, as is the potential damage to other fisheries resources and to healthy ecosystem functioning (Stevens et al., 2000; Kitchell et al., 2002; Ward and Myers, 2005; Myers et al., 2007). This chapter presents an overview of the major threats to pelagic elasmobranchs and the conservation status of the 12 species covered in this volume.

Threats Commercial fishing – both targeted and incidental – represents the greatest source of human-induced mortality for pelagic elasmobranchs. Fishing can affect population status directly, such as through a reduction in abundance or mean body size, or indirectly, through shifts in ecosystem structure and function (Stevens et al., 2000). Other than the pelagic stingray, all species considered in this volume are used locally as well as traded internationally for their meat, fins, oil, cartilage, or other products (Camhi et al., 2008b), although it is likely that only the demand for fins and meat would drive targeted pelagic shark fisheries. Shortfin mako, threshers, porbeagle, and silky, oceanic whitetip, and blue sharks are commercially targeted in various parts of the world (Vannuccini, 1999; CITES, 2004; Camhi et al., 2008b). In 2004, the white shark was listed on CITES Appendix II (Convention on

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International Trade in Endangered Species), which strictly regulates but does not ban the trade in white shark products. Given their oceanic habits and distribution, pelagic elasmobranchs are taken largely by industrial fishing vessels capable of spending extended periods at sea. These fleets, often equipped with freezer capability, use longlines, gill nets, and purse seines (in tropical waters) to target tunas and billfish. High-seas longline fisheries account for as much as 80% of the elasmobranch catch (by weight; Bonfil, 1994). Although the use of large-scale drift nets on the high seas was banned in 1992 by the United Nations (Resolution 44/225), gillnet fisheries still operate in the offshore waters of many countries. In some regions, where deep waters adjacent to narrow continental shelves bring pelagic fishes nearer to shore, artisanal fisheries can also take pelagic sharks in significant numbers (Bonfil, 1997). Historically, few offshore and high-seas fleets targeted pelagic sharks. More commonly, pelagic sharks were and are still taken as bycatch in a wide variety of fisheries. They are often the most significant bycatch species (by both weight and numbers) in pelagic longline and net fisheries targeting tunas and swordfishes in offshore domestic waters and on the high seas. In some of these fisheries, pelagic shark bycatch may even exceed the targeted catch (Camhi, 1999; Francis et al., 1999). Today, however, as the value and demand for shark fins continue to rise, many countries support fisheries that target pelagic sharks (Camhi et al., 2008b). Increasingly, the distinction between targeted and bycatch fisheries is becoming blurred (Clarke, 2003), as some fisheries shift to target sharks seasonally or even daily when the traditional target is less abundant (Aires-da-Silva et al., 2008; Hazin et al., 2008) and to take advantage of the lucrative fin trade (Camhi, 1999). Species-specific estimates in the Hong Kong fin markets suggest that 7–25 million pelagic sharks may be taken annually to support this trade (Clarke et al., 2006a, b). Full utilization of pelagic sharks may take place in some nearshore fisheries of major shark-fishing nations, but shark meat production remains minor relative to the demand for fins for most species (Clarke, 2003). Pelagic sharks, particularly shortfin mako, blue, porbeagle, and thresher sharks, are also highly valued by big-game anglers. Mako and threshers are often retained because of their high-quality meat, while blue sharks are usually released. Significant recreational fisheries for these species exist in Australia, New Zealand, the United States, the United Kingdom, and Ireland, as well as other nations (Babcock, 2008). Regardless of the location, the mortality of pelagic sharks at the hands of anglers is likely only a fraction of that taken in commercial fisheries, especially because angling and tournaments increasingly practice catch-and-release. Nonetheless, if there is a significant amount of post-release mortality for sharks that are caught and released by anglers, recreational fisheries could be a significant source of mortality that warrants monitoring and management. Other threats, although less important than fishing, can exacerbate negative impacts on pelagic elasmobranchs (Walker, 2002). Beach protection programs designed to reduce the risk of shark attack to bathers occur relatively close to shore. However, declines in the local abundance of some pelagic sharks that enter coastal waters, including white sharks, have resulted from netting operations off Australian, New Zealand, and South African beaches (Reid and Krogh, 1992; Dudley and Gribble, 1998; Smale, 2008). In comparison to coastal species, mating, pupping, and nursery areas for most pelagic sharks occur farther offshore but are poorly known and therefore difficult to protect. Given their wide-ranging and pelagic distribution, open ocean elasmobranchs are less likely than coastal species to be

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affected by habitat disturbances, such as from fishing gear or coastal development and runoff. However, some pollutants, including heavy metals and organic chemicals, bioaccumulate in the tissues of top predators. Mercury, for example, from background and industrial sources, occurs in high concentrations in some large pelagic sharks (Davenport, 1995), and as a neurotoxin it poses a health threat to sharks as well as to humans consuming these species (Moore, 2000). On a larger scale, the potential effects of global climate change, including warming ocean temperatures and ozone depletion, remain largely unknown; such changes will likely affect entire marine ecosystems, for example, by impacting the population dynamics of species that feed on phytoplankton and by changing species ranges and migratory patterns. Unsustainable fishing, in addition to being the major direct threat to most pelagic elasmobranchs, can interact with these environmental changes and lead to greater cumulative harm to the ecosystem (e.g., Bakun and Weeks, 2006). Fishing, however, is already within our ability to regulate, which is clearly necessary if we are to improve the conservation status of pelagic elasmobranchs.

Conservation status The status of pelagic elasmobranchs is less well known than that of coastal species. Historically, most pelagic sharks were taken as bycatch and usually discarded, which provided little impetus for fishery managers to require information collection on these catches. Conservation concerns, however, are beginning to shift managers’ perspectives on the need for shark data collection. A number of fishing nations (e.g., United States and Japan) now require better logbook reporting at the species level for both targeted catch and bycatch taken by their pelagic longline and net fisheries. Because of the multinational nature of pelagic shark movements and fisheries, regional fishery management organizations (RFMO) are also requiring better bycatch data reporting to facilitate population assessments and future management measures. The current lack of data, however, means that most evaluations of the status of pelagic shark populations are based on standardized catch rates rather than sophisticated population assessments. Of the pelagic elasmobranchs, the porbeagle of the Northwest Atlantic was the first species to undergo a formal stock assessment (Campana et al., 2008). The International Commission for the Conservation of Atlantic Tunas (ICCAT) held its first assessment for blue and shortfin mako sharks in June 2004; however, the catch data were incomplete and the findings are still considered preliminary (ICCAT, 2005; Babcock and Nakano, 2008). Stevens (2000) reviewed the population status of oceanic sharks in the Pacific, and some assessment work has also been done on blue sharks in the Pacific (Kleiber et al., 2001; West et al., 2004). Despite data limitations, qualitative assessments of the status of many commercially important elasmobranchs have been undertaken by the Shark Specialist Group of the World Conservation Union (IUCN) for inclusion on IUCN’s Red List (www.iucnredlist.org; IUCN, 2006; Fowler et al., 2005). These detailed status evaluations incorporate all available biological and fisheries data, and are based on extensive expert consultation. Although a global status evaluation is required for all species, geographically distinct populations may also be evaluated if appropriate data exist. The Red List confers no protected status

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Table 33.1 Global status of pelagic sharks and rays (Castro et al., 1999; IUCN, 2006). Scientific name

IUCN 2006 Red List Category (criteria)a

Population

Alopias pelagicus Alopias superciliosus Alopias vulpinus

VU (A2d⫹A4d) VU (A2bd) VU (A2bd⫹A3bd⫹A4bd) NT VU (A1cd⫹2cd) VU (A2abcd⫹A3bcd⫹A4acd) VU (A2bd⫹A3d⫹A4bd) LC VU (A2bd⫹3d⫹4bd) CR (A2bcd⫹3d⫹4bd)

Global Global Global California Global Global Global Global Global Northeast Atlantic Northwest Atlantic Mediterranean Southern Hemisphere Global North Indian, Tropical Pacific and Northwest Atlantic Global Northwest and western Central Atlantic Global Global

Carcharodon carcharias Isurus oxyrinchus Isurus paucus Lamna ditropis Lamna nasus

EN (A1abd) CR (A2bd) NT Carcharhinus falciformis

NT DD

Carcharhinus longimanus

VU (A2ad⫹3d⫹4ad) CR (A2bd⫹3bd⫹4bd)

Prionace glauca Pteroplatytrygon violacea

NT LC

Year assessed 2007c 2007c 2007c 2004 2000d 2007c 2005 2007c 2005 2005

FAO categoryb Category 3 Category 3 Category 4 Category 3 Category 4 Category 3 Category 1 Category 4

2005 2005 2005 2007c 2000d

Category 3

2005 2005

Category 3

2000d 2007c

Category 3 Not evaluated

a Red List categories (IUCN, 2006): CR: critically endangered; EN: endangered; VU: vulnerable; NT: near threatened; LC: least concern; DD: data deficient; see www.iucnredlist.org for further explanation of categories and criteria. b FAO categories (Castro et al., 1999): 1: Exploited but lack of data precludes inclusion in other categories; 3: exploited with limited reproductive potential, and/or vulnerable life-history traits, and/or being fished in their nursery areas; 4: shows substantial historical declines in catches and/or has become locally extinct. c Assessment done at Shark Specialist Group Red List workshop in February 2007, and awaits IUCN approval. d An updated assessment is being prepared.

but rather serves as a red flag that can help initiate or improve conservation and management for the listed species and populations. Of the 547 species of sharks evaluated for the 2006 Red List, IUCN found that 20% were threatened with extinction (IUCN, 2006). A Red List workshop in February 2007 specifically assessed the conservation status of oceanic sharks. A separate assessment of shark status was also undertaken by the Food and Agriculture Organization (FAO) (Castro et al., 1999). A number of pelagic sharks were found by both FAO and IUCN to be at risk of overexploitation, including blue, thresher, mako, porbeagle, salmon, silky, oceanic whitetip, and white sharks (Table 33.1). There are no reliable estimates of the number of pelagic sharks that remain in the world’s oceans, but recent studies (e.g., Baum et al., 2003; Baum and Myers, 2004) are shedding new light on the negative effects of fishing on these species. Although some of these studies have been criticized for being overly pessimistic given the limitations of available data and analyses (Burgess et al., 2005), they report declines similar to those found by other authors for some of the same pelagic (Baum et al., 2005; Campana et al., 2008; Hueter and

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Simpfendorfer, 2008) and large coastal shark populations (Cortés et al., 2006). All of these studies have raised awareness of both the research and conservation needs of pelagic sharks. The following sections briefly summarize the available information on catch trends and status assessments for 12 pelagic elasmobranchs.

Bigeye thresher Relatively little is known about the status of thresher sharks: As recent as 2006, the IUCN Red List classified all three species as Data Deficient (IUCN, 2006), but their status has recently been reevaluated. Threshers, especially the common thresher, are less likely than other sharks to be discarded at sea because of the palatability of their meat (Rose, 1996; Smith et al., 2008b), as well as the demand for their fins (Subasinghe, 1992, in Rose, 1996; Clarke, 2003). Among the three, the bigeye thresher (Alopias superciliosus) may be the most vulnerable because of its very low reproductive potential (2–3% per year; Smith et al., 2008b) and because it is regularly encountered in longline and net fisheries throughout the tropics and temperate regions. Although it is taken in large but poorly documented numbers both as a target and in bycatch, its global status remains uncertain, but large declines in catch per unit effort (CPUE) have been reported in the Northwest Atlantic (Table 33.2; Baum et al., 2003). An evaluation of its global status was undertaken in 2007 for the IUCN Red List and the bigeye thresher was determined to be Vulnerable. Castro et al. (1999) stated that a lack of fisheries data made it difficult to evaluate the status of this species, but they also indicated that its slow growth, low reproductive potential, and prevalence in longline bycatch made the bigeye thresher vulnerable to exploitation (Category 3).

Pelagic thresher The pelagic thresher (Alopias pelagicus; Table 33.1) is also not well studied. This species is readily caught in gill nets and on longlines, and in particularly high numbers in tuna fisheries throughout the waters of Southeast Asia (Chen et al., 2002), the northwestern Indian Ocean, and the western and central Pacific (Williams, 1999), as well as off the western coast of North America (Hanan et al., 1993). In Mexico, between the late 1980s and late 1990s, declines of up to 78% were documented off the Pacific Coast (Table 33.2; Mendizábal y Oriza et al., 2002, as cited in Sosa-Nishizaki et al., 2008). However, few fishery data are available from other regions. In 2007, the global status of the pelagic thresher was considered to be Vulnerable. Castro et al. (1999) highlighted its Vulnerability and suggested that the pelagic thresher cannot support intensive exploitation.

Common thresher The moderately productive common thresher (Alopias vulpinus), the most productive of the three threshers, is widely distributed along continental shelves in temperate waters of all oceans, and is taken in large numbers in directed fisheries and as bycatch. A California drift gill-net fishery targeting this thresher in the 1980s was unsustainable: Within a decade, landings had dropped by more than 70% (Cailliet et al., 1993) and average size declined by 25% between 1982 and 1989 (Hanan et al., 1993). This population is still recovering despite

Table 33.2 Trends in pelagic elasmobranch catch rates. Trend

Extent and time frame

Data

Region

Reference

Alopias pelagicus

↓

78%; late 1980s to late 1990s

CPUE

Pacific Mexico

Alopias superciliosus* Alopias vulpinus* Carcharodon carcharias

Northwest Atlantic Northwest Atlantic Northwest Atlantic KwaZulu-Natal, South Africa New South Wales, Australia New South Wales, Australia North and South Atlantic

Isurus spp.

↓

80%; 1986–2000 80%; 1986–2000 79%; 1986–2000 ⬎60%; 1978–1999 ⬎70%; 1950–1999 95%; 1961–1990 50% or greater in North Atlantic; less in South Atlantic; 1971–2002 45% in North Atlantic 1950s to late 1990s 73%; 1986–1997

Standardized logbook CPUE Standardized logbook CPUE Standardized logbook CPUE CPUE in beach protection nets

Isurus oxyrinchus

↓ ↓ ↓ ↓ ↓ ↓ ↓

Mendizábal y Oriza et al. (2002) as cited in Sosa-Nishizaki et al. (2008) Baum et al. (2003) Baum et al. (2003) Baum et al. (2003) Dudley (2002) Malcolm et al. (2001) Pepperell (1992) ICCAT (2005), Babcock and Nakano (2008)

↓ Isurus paucus Lamna ditropis

na Stable

Lamna nasus

↓

80–90% since 1960s

Carcharhinus falciformis

↓

91%; 1950s to late 1990s

Carcharhinus longimanus

↓

99%; 1950s to late 1990s

↓

70%; 1992–2000

Sport fishery shark catches Standardized commercial longline CPUE Standardized research and observer CPUE Standardized logbook CPUE

Standardized commercial longline CPUE Standardized research and observer CPUE Standardized research and observer CPUE Standardized logbook CPUE

Gulf of Mexico

Baum and Myers (2004)

Atlantic, Caribbean and Gulf of Mexico

Cramer (2000)

Northeast and Northwest Pacific Northwest Atlantic

Goldman and Musick (2008), Goldman (2002) Campana et al. (2008)

Gulf of Mexico

Baum and Myers (2004)

Gulf of Mexico

Baum and Myers (2004)

Northwest Atlantic

Baum et al. (2003)

Conservation Status of Pelagic Elasmobranchs

Species

(Continued)

403

404

Species

Trend

Extent and time frame

Data

Region

Reference

Prionace glauca

↓

Standardized research CPUE

Northwest Atlantic

Above MSY

80%; mid-1980s to early 1990s (males only) 1971–2002

North and South Atlantic

Stable

1971–2003

Standardized commercial longline CPUE Standardized logbook CPUE

Hueter and Simpfendorfer (2008), Simpfendorfer et al. (2002) ICCAT (2005), Babcock and Nakano (2008) Nakano and Clarke (2005)

↓

⬎86%; early 1950s to late 1990s Possible 5-fold; mid-1980s to mid-1990s 60%; 1986–2000 Early 1970s to early 1990s

Standardized observer and research CPUE

20%; early 1970s to early 1990s Late 1960s to early 1990s

Standardized logbook CPUE

↓ ↓ Stable ↓ Stable Pteroplatytrygon violacea

Standardized logbook CPUE Standardized logbook CPUE

Research and training vessel CPUE

na

*Baum et al. (2003) combines these two threshers to get a general trend. na: not available.

North Atlantic, South Atlantic and entire Atlantic Tropical Central Pacific

Ward and Myers (2005)

East coast of Australia

Stevens (2004)

Northwest Atlantic South Pacific, North and South Atlantic and Indian North Pacific

Baum et al. (2003) Nakano (1996) Nakano (1996)

North Pacific

Matsunaga and Nakano (1996)

Sharks of the Open Ocean

Table 33.2 (Continued).

Conservation Status of Pelagic Elasmobranchs

405

greatly reduced fishing pressure (Smith et al., 2008b). Similarly large declines in abundance based on logbook catch-and-effort data have been reported for the Northwest Atlantic (Table 33.2; Baum et al., 2003). Overall, however, little is known of the fisheries, stock structure, or status of common threshers in other areas (Goldman, 2005). In 2007, experts in the IUCN Shark Specialist Group evaluated the common thresher as Vulnerable on a global basis with a Near Threatened status in California waters (Table 33.1; IUCN, 2006). Castro et al. (1999) gave this species a Category 4 listing, because it has a low reproductive potential, is being targeted widely in intensive fisheries, and has suffered substantial decline under fishing pressure.

White shark Among the lamnids, the white shark (Carcharodon carcharias) is probably the most depleted by fishing on a global basis. Although widely distributed, the white shark is rare wherever it occurs. They suffer mortality in both targeted (uncommon in commercial fisheries but prized as a game fish) and bycatch fisheries. This mortality, coupled with their low productivity (Smith et al., 1998), has led IUCN to list white sharks as globally Vulnerable and possibly even Endangered as further status data are collated (Table 33.1; CITES, 2004; IUCN, 2006). Castro et al. (1999) placed white sharks in their Category 3 rather than a higher threat category, largely because there were few studies prior to 2000 that demonstrated population decreases. However, quantitative studies of white shark trends since then suggest clear declines in abundance ranging from 60% to 95%, along with declines in average size (Table 33.2; CITES, 2004). It is significant that no study to date has demonstrated long-term stable or increasing trends for this species (Wildlife Conservation Society, 2004). The rare and declining status of white sharks led to its listing as Vulnerable under Australia’s Endangered Species Protection Act in 1997, as well as to its protection in a number of other countries (Camhi et al., 2008a), making it the only pelagic shark with significant protected status. In 2004, driven by concerns over international trade in white shark fins, jaws, and teeth, this species was listed on Appendix II of CITES to monitor trade in its products and ensure that such trade does not contribute further to white shark decline (CITES, 2004). Studies are needed to determine the effectiveness of these protections in reversing population declines. Despite full protection in US Atlantic waters since the late 1990s, evidence has recently surfaced of significant illicit trade of white shark fins from this region. This suggests that legislative protection without corresponding monitoring and enforcement efforts provides only limited conservation benefit, even for high-profile, distinctive shark species like the white shark (Chapman et al., 2003; Shivji et al., 2005).

Shortfin mako The wide-ranging shortfin mako (Isurus oxyrinchus) is so highly valued for its meat (Rose, 1996) that, unlike other pelagic sharks, it is almost always retained when caught as bycatch as well as in targeted fisheries (Stevens, 2008). In addition, it is a highly sought and retained game fish (Babcock, 2008; Skomal et al., 2008). Although the shortfin mako has a slightly higher population growth rate than a number of other pelagic sharks (Smith et al., 2008a), it is still highly vulnerable to fishing pressure. Despite its economic importance in the meat

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and Hong Kong fin trade (Clarke, 2003), relatively little is known of its population status. The shortfin mako is listed in FAO Category 4 (Castro et al., 1999) and until recently was globally ranked as Near Threatened by IUCN (IUCN, 2006). However, worrying declines in the Atlantic led to its reevaluation as globally Vulnerable in 2007 (Table 33.1). The first multinational assessment for Atlantic mako sharks was conducted in 2004 by ICCAT. Although the results were highly uncertain, this shark has declined over the past three decades in both the North and South Atlantic, and may be overfished in the North Atlantic (Table 33.2; ICCAT, 2005; Babcock and Nakano, 2008). A more localized assessment in the Northwest Atlantic found moderate declines in makos based on US pelagic longline logbook data (Baum et al., 2003), and about a 50% decline based on unstandardized catch rates (for both makos combined) from the Gulf of Mexico between the 1950s and 1990s (Baum and Myers, 2004). Cramer (2000) reported a 73% decline in mako abundance in the US Atlantic Caribbean and Gulf of Mexico from 1986 to 1997 based on standardized catch rates from US logbooks.

Longfin mako The larger longfin mako (Isurus paucus) is more rarely encountered, and is more often discarded because its meat is of low quality. Limited to tropical and warm temperate seas, it is relatively uncommon in most waters. The longfin mako is globally ranked as Vulnerable (Table 33.1; IUCN, 2006; Category 3, Castro et al., 1999) because it is believed to have undergone significant declines in the Atlantic and is vulnerable to overfishing by the same tuna and swordfish fisheries taking shortfin makos. Improved catch data are needed to enable a more precise assessment.

Porbeagle The porbeagle (Lamna nasus) is a wide-ranging species with relatively discrete populations in cooler waters of the Northern and Southern Hemispheres (Francis et al., 2008). It is commercially valuable but highly vulnerable because of its low reproductive potential (Smith et al., 2008a). Porbeagles of the North Atlantic provide the most complete picture we have of the effect that fishing can have on a pelagic shark (Campana et al., 2002, 2008), and it is not an optimistic one. The fishery for porbeagles began in the Northeast Atlantic in the 1930s. Fishing was intense and unregulated, and collapsed in the 1960s (Gauld, 1989). In 1961, much of the effort shifted to the virgin Northwest Atlantic population, which also collapsed in the 1960s and again in the 1990s, despite precautionary management by the Canadian government beginning in 1994 (Campana et al., 2008). In May 2004, the Committee on the Status of Endangered Wildlife in Canada (COSEWIC) recommended that Canada designate the porbeagle as Endangered, based on their finding that fishing had driven the Northwest Atlantic porbeagle population to about 11% of its 1961 virgin biomass (Table 33.2; COSEWIC, 2004; Campana et al., 2008). Canadian scientists estimate that in the absence of fishing, population recovery could take about 30–60 years, but will take much longer if even low levels of mortality (e.g., bycatch) persist (DFO, 2005). In September 2006, the Canadian government declined to add the porbeagle to its List of Wildlife Species at Risk, citing primarily economic and monitoring reasons

Conservation Status of Pelagic Elasmobranchs

407

(Anonymous, 2006). In the Northeast Atlantic, the porbeagle has been depleted to as low as 5% of its initial biomass, prompting the International Council for the Exploration of the Seas (ICES) in 2005 to advise that no fishing should be allowed on this porbeagle stock (ICES, 2005). In 2005, the porbeagle shark was listed as globally Vulnerable on the IUCN Red List, with populations ranging from Near Threatened in the Southern Hemisphere, to Endangered in the Northwest Atlantic, to Critically Endangered in the Northeast Atlantic and Mediterranean (Table 33.1; IUCN, 2006). Much less is known of the historic porbeagle fisheries and catch trends in the Southern Hemisphere.

Salmon shark Salmon sharks (Lamna ditropis) were once thought to be limited to the boreal waters of the North Pacific, but recent satellite tracking revealed that they are highly vagile and range into the subtropics (e.g., Hawaii; Weng et al., 2005). In boreal waters, they are taken mainly as bycatch in salmon trawl and purse-seine fisheries and on longlines (Goldman and Musick, 2008), but fisheries interactions with this species at lower latitudes are currently unknown. The salmon shark is similar in its low productivity to pelagic thresher, silky, and porbeagle sharks (Smith et al., 2008a), and therefore may be extremely vulnerable to fishing mortality (Goldman and Human, 2005). Unlike its congener, however, much less is known of its catch statistics and abundance. As a result, the salmon shark could not be evaluated by Castro et al. (1999; Table 33.1) and IUCN listed it as Data Deficient until 2006 (IUCN, 2006). However, populations in the eastern and western North Pacific are believed to be stable (Table 33.2; Goldman, 2002; Goldman and Musick, 2008) and IUCN recently reevaluated its status as Least Concern globally.

Silky shark Silky sharks (Carcharhinus falciformis) are taken in large numbers in both targeted multispecies fisheries and as bycatch in tropical coastal and oceanic waters of all the world’s oceans (Bonfil, 2008). Silky sharks are second in importance only to blue sharks in the bycatch of western tropical Pacific longline tuna fisheries (Williams, 1999), as well as in the Hong Kong fin trade (Clarke, 2003). In some tropical fisheries, silky shark landings are even higher than for blue sharks, such as in the tuna longline and drift gill-net fisheries of Sri Lanka (Joseph, 1999). Despite these large catches, very little is known about silky population sizes or trends in abundance (Bonfil, 2008). A recent study, however, suggested a 91% decline in silky shark abundance in the Gulf of Mexico since the 1950s (Table 33.2; Baum and Myers, 2004). Silky sharks are only moderately productive, with an annual rate of population increase of about 4% (Smith et al., 2008a). Silky sharks were assigned to FAO’s Category 3, because of their biological vulnerability and prevalence as bycatch; a lack of fisheries trend data precluded a higher category of risk (Table 33.1; Castro et al., 1999). Although assessed by IUCN in 2000 as a species of Least Concern on a global basis, and Data Deficient for populations in the northern Indian Ocean, Northwest Atlantic, and tropical Pacific (IUCN, 2006), documented declines in the Atlantic indicate that this species is indeed susceptible to overfishing. However, in 2007,

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experts in the IUCN Shark Specialist Group reevaluated this assessment and designated the silky shark as Near Threatened globally.

Oceanic whitetip shark The oceanic whitetip (Carcharhinus longimanus) is one of the most common predatory fishes in oceanic tropical waters. Taken primarily as bycatch in tropical tuna fisheries, the relative importance of this species in the bycatch, as well as their retention and discard rates, varies widely by fishery (Bonfil et al., 2008). Although fins of the oceanic whitetip are preferred by Hong Kong fin traders (Rose, 1996), oceanic whitetips represent ⬍2% of the identified fins (Clarke et al., 2006b). This species falls at the upper range of pelagic shark productivities, but at only 4–6% per year it is still quite low compared to the teleosts targeted in the same fisheries (Smith et al., 2008a). Limited fisheries data preclude quantitative assessments in most waters. However, the oceanic whitetip was estimated to have declined by as much as 99% in the Gulf of Mexico since the 1950s (Table 33.2; Baum and Myers, 2004) and by 70% since 1992 in the Northwest Atlantic (Baum et al., 2003). In 2005, IUCN updated its status assessment for the oceanic whitetip, which was given a global status of vulnerable (Table 33.1), with the populations in the Northwest Atlantic and western Central Atlantic listed as Critically Endangered (IUCN, 2006).

Blue shark The blue shark (Prionace glauca) may be the most abundant pelagic shark in the ocean (IUCN, 2006; Nakano and Stevens, 2008). Because it is also one of the most wide-ranging sharks, found in both temperate and tropical seas from 60ºN to 50ºS, it is usually the most important shark in the bycatch of pelagic longline and net fisheries. The low desirability of blue shark meat (Rose, 1996), coupled with the relatively high value of its fins (Vannuccini, 1999), has led to the widespread practice of blue shark finning. Indeed, the blue shark is the most important species in the Hong Kong shark fin trade, composing more than 17% of the identified fins (Clarke et al., 2006b). This equates to as many as 16 million blue sharks killed annually for their fins. Overall mortality, however, is likely much higher than reported: In Canada, for example, reported blue shark landings may only be about 5% of their actual catch and mortality (Campana et al., 2005). The population status of blue sharks, because of their prevalence in offshore and highseas catches, is the best studied of the pelagic elasmobranchs (except for the Northwest Atlantic porbeagle population). For example, West et al. (2004) compiled an extensive summary of all available catch-and-effort data from the Pacific since the 1950s in an effort to assess the status of the blue shark. Many fishery managers believe that blue sharks are resistant to overfishing because of their abundance, widespread distribution, and moderate productivity, which ranges from 3.5 to 6.6% per year (Smith et al., 2008a). While some populations appear to be stable (Kleiber et al., 2001), recent studies suggest that blue sharks have indeed undergone large declines in some regions (Table 33.2). In the western North Atlantic, for example, fisheryindependent survey data indicate that male blue sharks were reduced by as much as 80% between the mid-1980s and the early 1990s with no change in female CPUE (Hueter and Simpfendorfer, 2008). In the same region, catch rates of both sexes combined declined by

Conservation Status of Pelagic Elasmobranchs

409

60% since 1986 based on logbook data (Baum et al., 2003). In contrast, Nakano (1996) found no blue shark declines in the Atlantic or Indian Oceans. Campana et al. (2005) reported that blue shark abundance since 1995 and median size since 1987 had declined in the North Atlantic, but could not determine the extent of the decline. In 2004, ICCAT conducted the first assessment of Atlantic blue shark bycatch in the tuna and swordfish longline fisheries and found that both North and South Atlantic stocks were above a biomass that would produce maximum sustainable yield, although these results are very preliminary (Babcock and Nakano, 2008; ICCAT, 2005). Trends in the North Pacific based on Japanese fisheries data are also unclear: Matsunaga and Nakano (1996) found no significant changes in blue sharks, whereas Nakano (1996) noted a 20% decline over roughly the same period. However, a more recent study comparing scientific survey data from the 1950s with observer data from longline vessels in the 1990s found an 87% decline in blue shark abundance and a 58% reduction in mean blue shark body mass in the Central Pacific (Ward and Myers, 2005). While a recent assessment in the western South Pacific could not determine the sustainability of current blue shark catches by Australian fisheries, it suggested that annual removals may have to be ⬍4% of the unexploited biomass (of sharks 6 months and older) to be sustainable (West et al., 2004). Very little is known of the conservation status of blue sharks in the Indian Ocean. In light of the uncertain population trends but heavy fishing pressure, IUCN has listed the blue shark as Near Threatened on the Red List (Table 33.1; IUCN, 2006) and FAO places it in Category 3 (Castro et al., 1999).

Pelagic stingray Little is known of the population status of the pelagic stingray (Pteroplatytrygon violacea), as its catches are rarely reported in the bycatch of oceanic fisheries and it is not subject to management (Neer, 2008). However, observer data from an experimental longline fishery off California in the late 1980s found that pelagic stingrays accounted for 8–9% of the catch, with blue and mako sharks making up 62% and 29%, respectively (PFMC, 2003). Pelagic stingrays are a notable bycatch of the New Zealand tuna longline fisheries: By number, it ranked 22nd out of 73 recorded species caught (Francis et al., 1999). A recent study looking at changes in the pelagic fish communities of the tropical Pacific since the 1950s suggested that as top oceanic predators (e.g., blue sharks) have been fished out, smaller and formerly rarer species, like the pelagic stingray, have increased in abundance, possibly as a result of a release from predation (Ward and Myers, 2005). No catch trends are published for the pelagic stingray and it was not evaluated by FAO (Castro et al., 1999). Previously considered to be Data Deficient, in 2007 the IUCN Shark Specialist Group determined the pelagic stingray to be a species of Least Concern (Table 33.1). In general, all trend assessments to date for pelagic sharks have been crude (see Francis et al., 2001) and should be considered preliminary, except possibly for porbeagles in the Northwest Atlantic (Campana et al., 2008). Even for blue sharks, which are the best studied but most heavily fished of the pelagic elasmobranchs, it is still not possible to determine sustainable catch levels for this species in any ocean basin (West et al., 2004; ICCAT, 2005). Therefore, until further data collection and analysis significantly improve our understanding of these populations, precautionary fishery management should be implemented for all pelagic sharks.

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Discussion Fisheries – largely those targeting teleosts like tunas and swordfish – are the greatest source of mortality for pelagic sharks. Although makos, threshers, and porbeagles have high-quality meat, most pelagic sharks, especially blue sharks, are killed just for their fins. Discards at sea, and the resulting unreported mortality, may greatly exceed reported catches (Campana et al., 2005). Despite a growing conservation awareness among some fishing sectors (e.g., FAO, ICCAT), including recent bans on the practice of finning (Camhi et al., 2008a; Pikitch et al., 2008), prospects for pelagic sharks in many parts of the world remain dim. The burgeoning demand for shark fins and their trade, estimated to be growing at 6.1% per year, will continue to increase pressure on pelagic shark stocks, which contribute about one-third of the fins traded in Hong Kong (Clarke, 2004). In addition, many developing nations are encouraging the expansion of their artisanal and offshore fisheries (Barnett, 1997), and increased mechanization means greater access to open ocean resources including pelagic sharks. Our ability to assess the conservation status of pelagic elasmobranchs is limited by incomplete data on catch-and-effort, life history, and stock structure, a lack of data on discards and total mortality, and questions about the reliability of the data we do have. Few countries report the species composition of their pelagic shark bycatch, and reported landings probably greatly underestimate the total mortality even for fisheries that record shark catches, because of finning, other discards, and chronic underreporting (Campana et al., 2005). The blue shark is probably the most widely studied pelagic shark because of its prevalence in tuna and swordfish bycatch, but the porbeagle is the most fully understood in terms of population status. Whereas status evaluations have been largely limited to catch-rate analyses, the porbeagle of the Northwest Atlantic is the first and only pelagic elasmobranch that has been subject to an adequate population assessment (Campana et al., 2008). Preliminary assessments have also been done for blue and shortfin mako sharks in the Atlantic and for blue sharks in the Pacific, but these assessments have been hampered by the lack of available data. At the other end of the knowledge spectrum, virtually nothing is known of the status of pelagic stingrays. Efforts to improve species-specific monitoring of pelagic shark bycatch and landings, including increased observer coverage, are slowly expanding (Babcock and Nakano, 2008; Camhi et al., 2008b), but they have yet to result in a sufficient improvement in the quality and quantity of shark catch statistics to allow adequate assessments of the status of shark populations and the sustainability of their fisheries (ICCAT, 2005). Fishing nations must marshal the political will to invest technical and financial resources in pelagic shark research and management. Regardless of these data limitations, a relatively clear picture of pelagic shark status is emerging: Expectations of resiliency aside, the wide-ranging distributions, moderate reproductive output, and highly migratory behavior of pelagic sharks have not shielded them from overexploitation. Indeed, some of the sharks discussed here may be among the most threatened populations in the world. With the exception of salmon sharks, and some data sets for blue sharks, all available catch-trend data suggest moderate to severe population depletions for pelagic sharks, based on 50–90% declines in catch rates (Table 33.2). The trends for blue sharks are mixed, with some studies suggesting stability and others substantial declines. In general, most of these

Conservation Status of Pelagic Elasmobranchs

411

depletions have been very rapid, in some cases taking less than a decade. Recovery, however, can be very slow (Cortés, 2008), possibly decades even if directed fishing is eliminated (Campana et al., 2008). The conservation status assessments undertaken for the IUCN Red List are expert-driven, regularly updated, and raise concerns about the sustainability of pelagic shark populations subject to unfettered exploitation. All recently evaluated pelagic sharks are considered at risk on a global basis. All three threshers, white, both species of mako, porbeagle, and oceanic whitetip sharks are listed globally as Vulnerable. However, where data permit the evaluation of regional populations, many of these are in worse straits. For example, porbeagles in the Mediterranean and Northeast Atlantic are considered to be Critically Endangered, and they are Endangered in the Northwest Atlantic. The blue shark is listed as Near Threatened. The silky shark is currently listed as a species of Least Concern, but this species is due for reevaluation in light of more recent trend analyses (Bonfil et al., 2008). A lack of fisheries data has resulted in a Data Deficient listing for the salmon shark, and the pelagic stingray was recently assessed as a species of Least Concern by IUCN. The status evaluations done by FAO (Castro et al., 1999) predate much of the recently collated catch-rate information and are mainly precautionary. Most species were simply ranked as Vulnerable based on their life-history constraints coupled with their exploitation (Category 3) or history of declines (Category 4), while the status of the pelagic stingray was not evaluated. The North Atlantic porbeagle shark exemplifies the effect that exploitation can have on a highly migratory, wide-ranging pelagic shark. Unregulated fishing in the Northwest Atlantic led to population collapse not once but twice over the past four decades. Although the fishery has now been subject to about 10 years of increasingly stringent management and catch limits – rare for a pelagic shark – the population remains at only 11% of its virgin biomass. Scientists believe that recovery will require the suspension of directed fishing and severe limits on the number of porbeagle taken as bycatch. As a result, porbeagle has been considered for listing as Endangered under Canadian law. Sustainable levels of fishing have not been determined for most other pelagic shark populations. While West et al. (2004) suggested that maximum sustainable fishing mortality rates may be only a few percent by weight of the unfished biomass of the stock, even for the relatively abundant and productive blue shark, fishing on pelagic sharks continues virtually without constraint. More thorough and reliable assessments of the impacts of fishing and sustainable catch levels await improved species-specific life-history and catch and discard data throughout the species’ ranges (West et al., 2004; ICCAT, 2005). We cannot, however, wait for long-term time-series data and definitive population assessments before management is implemented on behalf of these species (Camhi et al., 2008a; Cavanagh et al., 2008). Most studies to date are pointing in the same direction – down – suggesting that pelagic sharks cannot sustain current fishing levels. The low productivity of pelagic sharks taken as bycatch in expanding fisheries targeting much more productive teleost fishes, coupled with the growing demand for shark fins and fish protein in general, means that fishing pressure will only intensify in the future. Bans on shark finning (if enforced) are an important step. But hard-learned lessons from the Northwest Atlantic porbeagle population argue that additional management measures, including precautionary catch limits and time-area closures that reduce bycatch, are essential if we are to conserve and restore the populations of our increasingly beleaguered pelagic sharks.

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Acknowledgments I thank Shelley Clarke, Claudine Gibson, Ken Goldman, and Sarah Valenti for providing information and Beth Babcock, Demian Chapman, Sonja Fordham, Ellen Pikitch, and John Thomas for their helpful comments on the manuscript.

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Chapter 34

Domestic and International Management for Pelagic Sharks Merry D. Camhi, Sonja V. Fordham and Sarah L. Fowler

Abstract Despite increased attention to shark conservation and research over the last decade, including widespread adoption of international shark finning bans, most pelagic shark populations remain at risk of serious depletion. Seven years after adoption of the International Plan of Action for Sharks, only three species have received international protection (through trade restrictions), and no oceanwide or regional catch limits of these highly migratory species have been imposed. Ongoing efforts to improve information on pelagic shark fishing and population status have yet to be translated into effective measures to slow or reverse the depletion of these biologically vulnerable species. Improving the conservation status of oceanic sharks will require immediate, cooperative management action – including precautionary limits on fishing where scientific advice is not available – at national, regional, and international levels. Key words: pelagic shark, oceanic shark, conservation, management, RFMO, CITES, CMS, IPOA, UNCLOS.

Introduction Sharks have historically been a low priority for fishery managers, particularly compared with more economically valuable pelagic fish such as tuna and swordfish (Bonfil, 1994; Rose, 1996). As a result, data on shark catches, landings, discards, and mortality are lacking and are rarely recorded to the species level, thereby limiting scientists’ ability to determine sustainable fishing levels. This is particularly true for developing nation fisheries, which are responsible for a large proportion of reported elasmobranch landings (Barker and Schluessel, 2005). Such problems are exacerbated for the pelagic sharks, as they venture farther offshore and are caught in many fisheries and by fishermen from many nations. Effective management for oceanic sharks is hampered by this lack of data, as well as by their highly migratory nature, low reproductive rates, relatively low value, and lack Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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of a vocal constituency. Too often, managers and the public have a perception that these wide-ranging, transoceanic migrants are immune to overfishing. In addition, although targeted fisheries are rapidly expanding (e.g., in the European Union; Hareide et al., 2007), pelagic sharks are still largely taken as bycatch in the world’s longline and net fisheries, where they are killed mainly for their fins, and discards are poorly recorded. In these mixed-species fisheries, a greater biological vulnerability, coupled with a lack of monitoring or fishing limits, results in sharks becoming depleted even while fishing for the target species remains sustainable (Musick et al., 2000). Moreover, pelagic sharks are taken in international waters and by multinational fisheries, where enforcement is lacking and limits on shark fishing are nonexistent. A growing body of evidence suggests that fishing has removed vast numbers of the oceans’ top predators as high-seas fisheries have proliferated over the past five decades (Baum et al., 2003). Catch-rate analyses from fisheries around the world show declines of 45–90% for many pelagic sharks, with no population showing an increasing trend (Camhi, 2008). These large-scale depletions in apex predators are leading to changes in oceanic ecosystem structure that are reverberating throughout marine food webs (Stevens et al., 2000; Ward and Myers, 2005; Myers et al., 2007), with as yet undetermined consequences for marine communities and associated fisheries. In 2004, the United Nations General Assembly (UNGA) declared that “there has been little progress with respect to the conservation and management of sharks since the adoption of the IPOA [International Plan of Action - Sharks] in 1999” (UNGA, 2006). The Food and Agriculture Organization (FAO) acknowledged that, despite the lack of quality fisheries data and disagreement over how far some populations have fallen, no highly migratory oceanic shark stocks are reported as underexploited or recovering, and concluded that “the situation of world oceanic shark stocks is definitely a source of serious concern” (Maguire et al., 2006). This chapter focuses on the conservation needs of open ocean sharks and provides an overview of current management actions at the international, regional, and domestic levels. The measures discussed herein apply only to the 12 elasmobranchs addressed in this volume; there are, however, other management measures in place for other pelagic and coastal shark species. Evaluation of the current status of management was largely limited to English language sources and so may not be comprehensive. The terms “pelagic,” “open ocean,” and “oceanic” are used interchangeably. Specific management recommendations to improve the status of these vulnerable transoceanic migrants are also provided.

Management tools available for pelagic sharks Until the recent prohibitions on finning, the taking of sharks on the high seas was a veritable free-for-all. Yet a wide array of management tools and strategies – the same as employed for the conservation of tunas and cod – are available to limit the targeted catch of pelagic sharks (see Walker, 2004). Because most pelagic sharks are still taken incidentally and often killed only for their fins, measures aimed at avoiding bycatch, promoting live release, and improving post-release survival are critically important.

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Fishing restrictions The full range of traditional fisheries management tools can be applied to oceanic sharks. These measures include catch limits (e.g., total allowable catches, quotas, bag limits) to limit overall mortality, minimum and maximum size limits to protect the most reproductively valuable individuals in a population, season/area closures to protect sensitive life stages and aggregations, restrictions on time spent fishing or vessel/gear size to limit fishing capacity and bycatch (Gilman et al., 2007), and regulations to reduce waste, such as bans on finning. While the line between targeted and incidental catch of pelagic sharks is blurring, many of these traditional restrictions can also be applied to reduce shark bycatch (e.g., by setting bycatch quotas or closing areas of high shark bycatch), but they should be complemented with more innovative means to improve fisheries’ selectivity, such as modifications to fishing gear and techniques (Erickson and Berkeley, 2008). Circle hooks are increasingly promoted over traditional J-hooks to reduce the hooking rate as well as post-release mortality of sea turtles on pelagic longlines (Watson et al., 2005), but a study of blue sharks (Prionace glauca) in the North Pacific suggests that circle hooks may not reduce shark bycatch (Yokota et al., 2006), and may even increase it (Watson et al., 2005). Research into techniques to remove sharks safely from purse seines and repel them from longlines with chemicals and magnets may hold more promise for sharks (www.sharkdefense.com/).

Prohibitions on finning The growing demand for shark fin soup, particularly from the burgeoning Asian middle class, has led to increased trade in shark fins, in which pelagic sharks figure prominently (Clarke, 2003; Clarke et al., 2006a). The high value of fins compared to the usually less valuable meat creates an economic incentive to kill sharks solely for their fins. Shark “finning,” the practice of slicing off a shark’s fins and discarding the carcass at sea, has been widely criticized by conservationists and governments as wasteful, irresponsible, and even cruel. From a fisheries management perspective, finning is likely to result in unsustainable fishing mortality, because storing only the fins allows fishermen to kill many more sharks per trip than when the carcasses are also retained. Finning bans serve as a logical and publicly popular first step to reducing waste and curbing mortality, especially when properly enforced, and can be justified without population assessments. To ensure sustainable exploitation, however, finning bans must be complemented by limits on shark catch. Since 2000, efforts to ban shark finning have gained momentum in both domestic and international waters (Pikitch et al., 2008). As of mid-2007, 19 countries plus the European Union and 9 regional fisheries management organizations (RFMOs) have implemented binding bans on shark finning in their waters and for fishing vessels under their purview (Table 34.1). The effectiveness of these finning bans, however, varies with their implementation details (IUCN, 2003). The most effective and enforceable means of banning finning is to require that sharks be landed with their fins still attached to their bodies (IUCN, 2003; Hareide et al., 2007). This approach, which also dramatically enhances the ability to collect much needed species-specific catch data, has been employed in only a few

Table 34.1 International, regional, and domestic prohibitions on shark finning (through June 2007; bans are mandatory unless otherwise stated). Date

Area

Implementationb

International FAO UNGA IUCN

1999 November 2004 November 2004

All waters All waters All waters

IPOA-Sharks: minimize waste and discards (voluntary). Resolution on Oceans and Law of the Sea discourages shark finning and encourages full utilization (voluntary). Recommendation 3.116 urges that all sharks be landed with fins intact and full utilization; otherwise, landed fins are not to exceed 5% of landed shark weight (voluntary).

Regional ICCAT

November 2004

GFCM IOTC IATTC NAFO SEAFO WCPFC

2005 May 2005 June 2005 September 2005 October 2006 December 2005

Atlantic, Mediterranean, and Gulf of Mexico Mediterranean Indian Eastern Pacific Northwest Atlantic Southeast Atlantic Western and Central Pacific

CCAMLR NEAFC

2006 2007

Antarctic waters Northeast Atlantic

Full utilization (only head, skin, and guts may be discarded); landed fins are not to exceed 5% of landed shark weight; recommends live release of incidentally caught sharks. Same measures as ICCAT. Same measures as ICCAT. Same measures as ICCAT. Same measures as ICCAT. Same measures as ICCAT. Same measures as ICCAT; initially applies to vessels ⬎24 m; currently voluntary, but measure becomes mandatory in January 2008. All directed fishing for sharks is prohibited; recommends live release of incidentally caught sharks. Same measures as ICCAT.

National Australiac,d

October 2000

Brazilc Canadac

August 1998 1994

Commonwealth (federal) waters, 3–200 miles offshore Brazil waters Atlantic and Pacific

Cape Verde Columbia Costa Rica

February 2005 June 2007 2001

Ecuador

October 2004

Egypt

August 2005

El Salvador

December 2006

Finning is prohibited in Ecuador waters and the sale or export of fins is strictly prohibited; targeted fishing for sharks is prohibited; incidentally caught sharks should be fully utilized. Shark fishing is prohibited throughout the Egyptian Red Sea to 12 miles offshore.

421

Cape Verde waters Columbia waters Costa Rica waters and wherever CR vessels fish All Ecuador waters, including Galapagos Egyptian territorial waters in the Red Sea (12 miles) El Salvador waters and wherever ES vessels fish

Finning is prohibited in tuna longline and all Commonwealth fisheries taking sharks; additional regulations apply in some territorial waters (out to 3 miles). Total weight of fins shall not exceed 5% of the total weight of carcasses. Finning is prohibited in Canadian waters and extends to any Canadian licensed vessel fishing outside the 200-mile EEZ; fins must not exceed 5% of dressed carcass landed weight. Finning is prohibited throughout EEZ. Sharks must be landed with fins intact. Permits for transporting and shipping fins. Sharks must be landed with fins attached to carcass.

Domestic and International Management for Pelagic Sharks

Entitya

Fins must remain at least one-quarter attached to the carcass. (Continued)

422

Table 34.1 (Continued). Date

Area

Implementationa

European Union (27 Member States) French Polynesia Israel Mexicoc

September 2003

EU waters and wherever EU vessels fish

April 2006 1980 Feb 2007

French Polynesia waters Israeli waters Mexican waters and wherever Mexican vessels fish

Finning is prohibited; fins must be landed attached to carcass; a “special fishing permit” allows fins to be landed or transshipped separately, if processing is undertaken onboard, but “in no case shall the theoretical weight of the fins exceed 5% of the live weight of the shark catch.” Finning is prohibited, as is the trade in all shark parts and products except for shortfin mako. All sharks have protected status in Israeli waters; shark fishing and, by default, finning are illegal. Finning is prohibited for all vessels, sharks may not be landed unless their carcasses are also onboard.

Namibia Nicaragua

Finning legislation pending? 2005

Oman

Prior to 1999

Palau

2003

Palau waters

Panama

March 2006

Panama waters

Seychelles

February 2006

Seychelles waters

South Africa

1998

Spainc

2002

United Statesc

March 2002 (since 1993 in Atlantic)

South Africa waters and wherever SA vessels fish Spain waters and wherever Spanish vessels fish US waters and wherever US vessels fish

Nicaragua waters including Lake Cocibolca

Currently, law prohibits dumping of biological materials in territorial waters, which should preclude, but does not specify, finning; in general, discards are prohibited. Fishing for sharks solely for their fins is prohibited; sharks must be landed with their corresponding carcasses; weight of fins shall not exceed 5% of the total landed weight of carcasses; to export fins, exporters must prove that they also marketed the meat. No waste of any shark part at sea or on land; fins and tails must remain attached to carcass; license needed to export or handle any shark part. Shark fishing is banned in State waters, as is finning by foreign vessels; all incidentally caught sharks must be released dead or alive. Commercial fisheries must land sharks intact; artisanal fisheries may land fins separately, but fins must not exceed 5% of the landed shark meat trade in fins requires certificate of origin. Finning is prohibited by foreign vessels fishing in Seychelles waters by requiring that the weight of fins shall not exceed 5% of the landed dressed carcass weight; does not apply to domestic vessels. Finning is prohibited; fins can be separated from carcasses but must be landed together with a fin-to-carcass (dressed-weight) ratio of 8% for domestic vessels and 14% for foreign vessels. Finning is prohibited; fins must be landed attached to carcass; a “special fishing permit” allows sharks to be landed separately, but fins must not exceed 5% of landed whole carcass weight. Finning is prohibited; fins must be landed with the corresponding carcass; fins must not exceed 5% of dressed carcass landed weight.

a Entities are: FAO = United Nations Food and Agriculture Organization; UNGA = United Nations General Assembly; IUCN = World Conservation Union; ICCAT = International Commission for the Conservation of Atlantic Tunas; GFMC = General Fisheries Commission for the Mediterranean; IOTC = Indian Ocean Tuna Commission; IATTC = Inter-American Tropical Tuna Commission; NAFO = Northwest Atlantic Fisheries Organization; SEAFO = South East Atlantic Fisheries Organization; WCPFC = Western and Central Pacific Fisheries Commission; CCALMR = Commission for the Conservation of Antarctic Marine Living Resources; NEAFC = North East Atlantic Fisheries Commission. b Refer to IUCN Web page (www.flmnh.ufl.edu/fish/organizations/ssg/ssg.htm) for further details and updates. c Major shark-fishing nation defined as reporting ⬎10,000 t of elasmobranch landings to FAO in 2004. d Finning also banned in six State and Northern Territory waters (to 3 miles).

Sharks of the Open Ocean

Entity

Domestic and International Management for Pelagic Sharks

423

countries, such as Costa Rica and parts of Australia. Because of industry’s interest in storing shark fins separately, most nations and all RFMOs regulate finning through a fin-tocarcass-weight ratio aimed at ensuring that the amount of fins corresponds to the amount of carcasses onboard (Table 34.1). Yet the appropriate fin-to-carcass ratio is subject to debate. The United States, Canada, and parts of Australia employ a 5% fin-to-dressedweight (or 2% of whole weight) ratio; data from these regions indicate that this value is an upper limit for mixed-shark fisheries (Cortés and Neer, 2006). Others, such as the European Union and Brazil, allow a much higher ratio of 5% of whole or “live” weight (which equates to 10% or more of dressed weight) and, in the EU case, are justified by data from Spanish and Portuguese longline vessels that indicate retention of the whole tail and significant amounts of meat along with fins. Such high ratios, if applied to fisheries that cut fins cleanly and keep only the lower lobe of tail (as the market demands), provide a possible loophole to fin sharks while remaining within the fin weight limit (IUCN, 2003). In addition, it is difficult and costly to monitor compliance with a weight ratio, particularly in the absence of at-sea observers (Hareide et al., 2007). The first RFMO finning ban, adopted by the International Commission for the Conservation of Atlantic Tunas (ICCAT) in 2004, included the ambiguous standard of fins not exceeding “5% of the weight of the sharks onboard” (ICCAT, 2004) in order to accommodate both of the foregoing ratios employed by member countries. The loophole created by not specifying ratios based on dressed weight and therefore allowing whole weight ratios has the potential to undermine the effectiveness of shark finning bans on a global scale. Within a few years, most of the world’s RFMOs had adopted identical, operative text in their own finning bans. Given regional differences in species and fin retention techniques, as well as related enforcement problems associated with ratios, requiring that sharks be landed with their fins attached appears to be the only means of ensuring that finning does not occur, as intended by the bans (Cortés and Neer, 2006).

Species protections Many nations attempt to conserve shark species of concern by declaring them “protected” or “prohibited” species, with the former usually more restrictive, either as a first step to or a substitute for fisheries management (Table 34.2). Too often, such action is reserved for the most charismatic or targetable species, such as the whale (Rhincodon typus), white (Carcharodon carcharias), and basking sharks (Cetorhinus maximus). Usually, such designations render it illegal to target or possess the protected species. These measures often mandate careful release of individuals taken as bycatch, but are rarely tied to initiatives to actually reduce their bycatch. It should also be noted that such restrictions usually do not rival protective measures or enforcement for marine mammals or sea turtles in terms of penalties. Still, a prohibition on possession of shark species of concern is a simple, relatively enforceable, and sometimes precautionary way to safeguard shark species at risk and to publicize the need to conserve them. Consideration of species protection can be triggered by government pronouncements that a species is endangered or of “special concern.” In Canada, porbeagle (Lamna nasus) and white sharks have been deemed “endangered” in Atlantic waters by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC), the authority for assessing

424

Scientific name

Common name

Alopias pelagicus Alopias superciliosus Alopias vulpinus Carcharodon carcharias

Pelagic thresher Bigeye thresher Common thresher White shark







Isurus oxyrinchus Isurus paucus Lamna ditropis Lamna nasus Carcharhinus falciformis Carcharhinus longimanus Prionace glauca Pteroplatytrygon violacea

Shortfin mako Longfin mako Salmon shark Porbeagle Silky shark








Oceanic whitetip




Blue shark Pelagic stingray




a

UNCLOS

CITES

CMS

RFMO focusa

Barcelona Conventionb

Domestic protectionc

US Atlantic and Gulf of Mexicod Appendix II

Appendices I, II

Annex II

Australia, Croatia, European Union (27 Members States), Malta, Mexico, Namibia, New Zealand, South Africa, and all US waters except in the western Pacific


US Atlantic and Gulf of Mexicod Proposed (2007)

Proposed (2007)

Annex III




Sweden

Annex III

Species subject to a population assessment at ICCAT. See Babcock and Nakano (2008). Barcelona Convention listings are not fully implemented; Annex II lists endangered or threatened species and Annex III lists species whose exploitation is regulated. c Ecuador, Egypt, Israel, Palau (for foreign vessels), and Republic of the Congo prohibit directed fishing for sharks in their territorial waters. d Species is prohibited from commercial and recreational fishing as opposed to being protected under endangered species laws. b

Sharks of the Open Ocean

Table 34.2 International treaties and domestic species-specific protection for pelagic elasmobranchs.

Domestic and International Management for Pelagic Sharks

425

extinction risk under the Species at Risk Act. To date, the need to consider economic factors has prevented these scientific findings from resulting in protective measures. Similarly, the US National Marine Fisheries Service recently added porbeagle sharks to its “Species of Concern” list; the economic effects of a government proposal to prohibit possession of the species are currently being weighed against the biological benefits of protection. Some nations have taken species protection a step further by prohibiting the targeted fishing of all elasmobranchs in some or all of their territorial waters. These include the Republic of the Congo, Ecuador, Egypt, Israel, and Palau (for foreign vessels only; Table 34.2).

International and regional management action Pelagic sharks are, by nature, highly migratory: They traverse the seas without regard for political boundaries. As a result, management efforts of one State can be undermined by actions or a lack of action in the waters of a neighboring State or on the high seas. Hence, the effective conservation of pelagic sharks requires management attention across their entire range and therefore depends on regional and international cooperation in data collection, management, and enforcement. The following sections briefly summarize the international and regional fishery and conservation instruments that are most relevant to oceanic sharks, and then describe what is being done to fulfill their mandate to ensure that fisheries are sustainable.

Fisheries agreements International treaties Instruments that address the conservation needs of oceanic fishes fall into two categories: legally binding (“hard law”) agreements that include fisheries and conservation treaties and conventions, and nonbinding (“soft law”) resolutions and guidelines. Binding agreements, such as the UN Convention on the Law of the Sea (UNCLOS), the UN Fish Stocks Agreement (UNFSA), and the treaties establishing the RFMOs, are obligatory on the Parties that sign them (Table 34.3). These legal instruments establish sustainability as a management goal and promote the “precautionary approach,” particularly when data are lacking, which is most frequently the case for pelagic sharks. For soft law agreements, such as the Code of Conduct for Responsible Fisheries (FAO, 1995), the IPOA-Sharks and the UN Driftnet Ban, implementation is voluntary. It is important to note, however, that while providing a framework, these international fisheries instruments do not translate directly into management action or enforcement – that is left to the RFMOs and individual fishing States to implement. Currently, there are no international or regional fishery bodies specifically dedicated to the management of pelagic sharks and no international or bilateral pelagic shark limits have been imposed. All pelagic sharks addressed in this volume are listed, however, as “highly migratory species” under Annex I of UNCLOS (Table 34.2), and thereby subject to its provisions. The 1995 Agreement for the Implementation of the Provisions of

426 Sharks of the Open Ocean

Table 34.3 Membership of major shark-fishing nations to RFMOs and international fisheries and conservation agreements, and year agreement entered into force.a Nation

Indonesia India Spaind Taiwane Mexico Argentina United States Thailand Pakistan Malaysia Japan Franced Brazil Sri Lanka

2004 elasmorbranch landings (t) 108,944 79,825 51,260 43,797 37,540 32,039 30,732 27,646 27,363 25,053 23,475 21,799 20,041 19,510

Fisheries agreements UNCLOS 1986 1995 1997

Fish Stocks Agreement 2003 2003

1983 1995 1996 1997 1996 1996 1996 1988 1994

2003 2000 1996

Conservation agreements b

Selected RFMO membership

IOTC, WCPFC IOTC ICCATf, GFCMg, IATTC, ICCAT, IATTC, CCSBT, WCPFC ICCAT, IATTC ICCAT, IATTC, WCPFC IOTC IOTC IOTC ICCAT, GFCM, IATTC, IOTC, CCSBT, WCPFC ICCATh, GFCMg, IATTC, IOTCh, WCPFCh ICCAT IOTC

NPOA-Sharks adoptedc

2006 2004 2001

2006 2001

CITES

CMS

1979 1976 1986

1983 1985

1991 1981 1975 1983 1976 1978 1980 1978 1975 1979

1992

1987

1990 1990 (Continued)

Iran New Zealand United Kingdomd Nigeria Portugald Yemen Korea, Republic of Canada Australia

18,318 16,647 16,066 13,560 12,765 12,750 12,265 11,841 11,459

1996 1997 1986 1997 1987 1996 2003 1994

1998 2001 2001

IOTC CCSBT, WCPFC ICCATh, IOTCh

2003

ICCATf

1999 1994

ICCAT, IATTC, IOTC, CCSBT, WCPFC ICCAT, IATTC, WCPFC IOTC, CCSBT, WCPFC

2007 2004

Major shark-fishing nation defined as reporting ⬎10,000 t of elasmobranch landings to FAO in 2004. See Table 34.4 for full names of these RFMOs. Italics indicates cooperating Non-Party or Cooperating Fishing Entity. c Only NPOAs adopted by April 2007 are indicated here. See Cavanagh et al. (2008) for further details on NPOA status. d Member of the European Union; together, the 27 Member States of the European Union landed 109,121 t of elasmobranchs in 2004. e Within the UN, Taiwan is not recognized as a separate government from the People’s Republic of China, which precludes their membership in UN agreements. f Member as part of the European Community, which is a cooperating Non-Party of the IATTC and CCSBT. g Individual member and member as part of the European Community. h Member as part of the European Community and on behalf of overseas territories.

1976 1989 1976 1975 1981 1997 1993 1975 1976

2000 1985 1987 1983 2006

1991

a

b

Domestic and International Management for Pelagic Sharks 427

428

Sharks of the Open Ocean

UNCLOS relating to the Conservation and Management of Straddling Fish Stocks and Highly Migratory Fish Stocks (UNFSA) builds upon UNCLOS obligations for high-seas fish populations by setting out mechanisms for cooperation among fishing nations, including the establishment of regional fisheries arrangements or organizations. In recent years, the UNGA has repeatedly urged nations and RFMOs to collect shark fisheries data and adopt shark management measures, particularly for vulnerable or threatened shark populations. In its fisheries resolutions, UNGA has also called for the conservation and long-term sustainable use of sharks, as well as bans on directed shark fisheries “conducted solely for the purpose of harvesting shark fins” and other means to minimize waste and encourage full use of dead sharks (UNGA, 2006). These statements and agreements have yet to translate directly into management action for sharks.

RFMOs RFMOs are charged with overseeing and regulating international and transboundary fisheries. Most of the world’s RFMOs are focused on fisheries for commercially valued species such as cod or tuna, and no RFMO has been established specifically to address the management needs of oceanic sharks. RFMOs with a mandate to manage tunas and tuna-like species are most relevant to pelagic sharks because they are obligated by their charters to address the effect that the target fisheries under their purview have on bycatch species, including sharks, seabirds, sea turtles, and other nontarget species (Table 34.4; Weber and Fordham, 1997; Small, 2005). A number of them have established bycatch or shark working groups to begin to address the needs of these species. Because RFMOs primarily respond to the interests of their most vocal constituents (industry) and are focused on management, allocation, and enforcement issues of their generally overfished target species, they have been slow to address the management needs of pelagic sharks. Since 2004, however, most of the world’s RFMOs have taken initial steps toward conservation of sharks and/or closely related skates and rays, with each standing out in a particular way. As discussed previously, most RFMOs have adopted finning bans, following the lead and model of ICCAT (2004). ICCAT was also the first to produce population assessments for pelagic sharks and to establish a working group specific to sharks (Babcock and Nakano, 2008). The Northwest Atlantic Fisheries Organization (NAFO) was the first RFMO to adopt an elasmobranch catch limit (for thorny skates) in 2004. Four years later, they remain the only RFMO to have done so. The Inter-American Tropical Tuna Commission (IATTC) is leading RFMOs in encouraging the prompt and careful release of all sharks and rays caught in all of its fisheries and in researching effective release methods (IATTC, 2007). In late 2006, the Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR, 2006) adopted a precautionary ban on directed shark fisheries until scientific advice for sustainable catch limits is developed and considered. To its finning ban in 2006, the Western and Central Pacific Fisheries Commission (WCPFC, 2006) added an option requiring that sharks be landed with their fins attached as an alternative to the 5% ratio, thereby acknowledging the best means to enforce such bans. The WCPFC shark resolution, however, currently applies only to vessels greater than 24 m in length. Many of the provisions of these RFMO shark resolutions beyond the finning bans, while laudable, are not mandatory (Lack and Sant, 2006). In particular, there is no guarantee

Table 34.4 Action for pelagic sharks taken by a subset of regional fisheries management organizations. RFMO (FAO fishing area)

Year in force

Number of membersa

Encourages live release of bycatch

Shark research plansb

GFCM

General Fisheries Commission for the Mediterranean (Area 37) International Commission for the Conservation of Atlantic Tunas (Areas 21, 27, 31, 37, 41, 47, 48) Inter-American Tropical Tuna Commission (Areas 77, 87)

1952

23 ⫹ European Union




1969

42 ⫹ European Union




1950

15




2004

16




1996

19 ⫹ European Union




Selective gear, identify nursery areas Assess blue and shortfin mako (ongoing); live release, identify nursery areas Preliminary status advice and research plan to study live release, selective gear, identify nursery areas Review fin ratio in 2007; encourages cooperative stock assessmentse Preliminary advice on status of key species; live release, identify nursery areas; review fin ratio

ICCAT

IATTC

WCPFC

IOTC

CCSBT

Western and Central Pacific Fisheries Commission (Areas 61, 71) Indian Ocean Tuna Commission (Areas 51, 57)

Commission for the Conser1994 vation of Southern Bluefin Tuna CCAMLR Commission on the 1982 Conservation of Antarctic Marine Living Resources (Areas 48, 58, 88) a

Finning ban/ Calls for promotes landings data full use by species

Catch limits for sharks




GFCM (2005)


/





ICCAT (2004)


/


Where possible

IATTC (2002, 2005, 2007)


d /





WCPFC (2006)


/





IOTC (2005)

na

Prohibits directed shark fishing

Lack and Sant (2006) CCAMLR (2006)

429

Includes Contracting Members only, but Cooperating Non-Members may also be important to the effectiveness of the RFMO in shark management. In most cases, recommended research “is encouraged” or “where possible” and has not yet been implemented. c No RFMO has yet proposed to draft and implement a regional Shark Plan of Action under the IPOA-Sharks, but some encourage their Member States to do so. d To implement finning ban, endorses landing of carcasses with fins attached. e These measures are currently voluntary and apply only to vessels ⬎24 m long; they become binding in January 2008. b

Reference




5 23 ⫹ European Union

Plan of Action (under IPOA)c

Domestic and International Management for Pelagic Sharks

Acronym

430

Sharks of the Open Ocean

that recommended research into selective gear, live release, and nursery habitat will actually be undertaken. Despite calls by ICCAT, IATTC, and other RFMOs for improved data collection on pelagic sharks taken in tuna fisheries, the root problems of under-reporting, misreporting, and species-level data amalgamation remain. To date, the only speciesspecific scientific advice to an RFMO regarding a pelagic shark has come from ICCAT’s Scientific Committee in 2005: to reduce fishing mortality on North Atlantic shortfin mako sharks (Isurus oxyrinchus). ICCAT Parties, however, have yet to take meaningful action on this advice, or on scientific advice from the International Council for Exploration of the Sea (ICES) to end fishing on Northeast Atlantic porbeagle sharks (ICES, 2006). ICCAT participants have criticized efforts to limit trade in porbeagle sharks through the Convention on International Trade in Endangered Species (see below) as an encroachment on ICCAT’s responsibility, yet Parties have stopped short of proposing any ICCAT action for the species. A lack of political will among RFMOs and their Member States to fulfill science-based recommendations may be the biggest impediment to improving the status of oceanic sharks (Willock and Lack, 2006). Finally, no RFMO has drafted a regional Shark Plan as directed by the IPOA-Sharks, nor have they established – or even recommended – concrete catch limits to cap mortality on increasingly targeted pelagic shark populations.

IPOA-Sharks The FAO Committee on Fisheries adopted the IPOA for the Conservation and Management of Sharks (IPOA-Sharks) in 1999. The IPOA highlights the action required for sharks within the context of the Code of Conduct for Responsible Fisheries. It calls on all fishing nations and RFMOs to carry out regular assessments of the status of their shark stocks. It also directs those nations whose fisheries take sharks to develop and implement a National Shark Plan in accordance with FAO technical guidelines (FAO, 2000). However, the IPOA is voluntary and cannot mandate action on the part of fishing nations. The developmental chronology of the IPOA and its implementation at the domestic level are discussed in detail by Cavanagh et al. (2008). Despite initial, widespread support for the IPOA-Sharks, progress toward implementation has been disappointingly slow: As of early 2007, only 7 of the 113 nations reporting elasmobranch landings have adopted their National Shark Plan, although at least 17 more are in the process of drafting their plans (Table 34.3; Cavanagh et al., 2008).

Wildlife conservation agreements The poor record of RFMOs in securing sustainable fisheries for the species under their purview, particularly bluefin tuna and billfishes as well as cod and flatfish, coupled with their lack of progress in safeguarding sharks, has encouraged conservationists and governments to look toward international agreements traditionally reserved for cetaceans, birds, and land mammals to address the conservation needs of depleted sharks. When compared to RFMOs and voluntary fishery agreements, these wildlife instruments often have much larger membership and can provide a stronger legal framework for addressing the

Domestic and International Management for Pelagic Sharks

431

conservation and trade needs of listed species (Table 34.3; IUCN, 2007). Two international wildlife treaties – the Convention on International Trade in Endangered Species (CITES) and the Convention on the Conservation of Migratory Species (CMS, or the Bonn Convention) – are particularly relevant for pelagic sharks given the substantial international trade in their parts and their highly migratory nature. These agreements could provide a complementary route for improving the conservation status of several oceanic sharks, but must be bolstered by shark fisheries management programs for optimum effectiveness. Similarly, the many Regional Seas Conventions (e.g., www.unep.ch/seas/) may oblige nations to take appropriate measures for the conservation and management of listed species. To date, only the Barcelona Convention has listed some Mediterranean pelagic sharks, but all could potentially do so.

CITES CITES provides an international legal framework to protect species at risk of overexploitation from international trade. Species in trade that are facing extinction may be listed on Appendix I, which essentially bans international trade in that species or its parts. Appendix II is reserved for species that could become threatened with extinction if trade is not controlled. Listing on Appendix II serves to monitor and limit trade to sustainable levels by requiring exporting countries to issue permits, and to do so only after documenting that such trade will not have a detrimental effect on the species’ population in the wild. Specific quantitative biological and trade criteria guide the CITES listing process (Fordham and Dolan, 2004). Currently, 170 countries are party to the CITES convention (www.cites.org/eng/news/party/sb_me.shtml). CITES has been a driving force in global shark conservation since 1994, when the Member Parties developed and adopted a resolution (Resolution Conference 9.17) highlighting the plight of sharks and directed the CITES Animals Committee to compile data on the biological and trade status of shark species subject to international trade. This directive resulted in a number of detailed reports focusing on the vulnerability of sharks to widespread yet poorly documented exploitation (Rose, 1996; Camhi et al., 1998). A Shark Working Group was formed by the CITES Animals Committee to provide regular advice to CITES Parties regarding proposed listings, species status, and fishery management priorities (Fordham and Dolan, 2004). Pelagic sharks are heavily exploited for international trade in shark fins. Nearly onethird of the identified shark fins traded in the Hong Kong fin market come from oceanic species, resulting in an annual mortality of an estimated 7–25 million pelagic sharks (Clarke et al., 2006a, b). Species such as the porbeagle and shortfin mako are prized for their meat as well, which also enters international trade (Fowler et al., 2004). CITES listings can complement existing management, particularly when international trade is a driving force behind a species’ depletion. In the case of sharks, however, listings have been sought as stop-gap measures in situations where fisheries management entities have failed to ensure the sustainable use of shark species in trade. In 2002, the first shark species – basking and whale sharks – were listed on CITES Appendix II. In 2004, the white shark was added (CITES, 2004). Another pelagic shark – the porbeagle – was proposed for listing on Appendix II at the 14th Conference was of Parties in June 2007. Although

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the CITES Secretariat endorsed this listing, the porbeagle failed to receive the two-thirds majority vote among Parties required for adoption. Parties that object to CITES listings have the option to file a “reservation,” in which case they are not bound by the listing provisions. Norway, Japan, and Iceland have voiced strong opposition to the listing of sharks under CITES Appendices and have taken reservations on all three listed shark species, including white sharks. Palau has also filed a reservation to the white shark listing. The conservation benefits of these CITES listings and the effect of these reservations have yet to be fully evaluated.

CMS CMS, also known as the Bonn Convention, acknowledges the need for conservation throughout a species’ range, including across domestic and international boundaries. Migratory species considered to be threatened with extinction are listed on Appendix I. CMS encourages domestic action by its Member States, as well as concerted action among Range States, aimed at strict protection, habitat conservation, and mitigation of obstacles to the recovery of the listed species. CMS Appendix II includes species with an “unfavorable conservation status” that would benefit from international cooperation. CMS encourages the Range States, both Parties and Non-Parties, to develop global or regional agreements ranging from legally binding agreements to less formal instruments, such as Memoranda of Understanding. Such plans can be adapted to the conservation needs of particular regions and species (CMS, 2003). Currently, three sharks are listed on CMS: The whale shark was listed on Appendix II in 1999, the white shark was listed on Appendices I and II in 2002, and in 2005 the basking shark was also listed on both Appendices. These listings contributed to the protected status for basking and white sharks in the European Union, and for white sharks in New Zealand. Several years after the whale shark listing, there still has been no regional cooperation for this species, although some Parties have expressed interest in developing a regional conservation plan in the Indian Ocean and the waters of Southeast Asia. The slow progress toward regional conservation agreements for these species illustrates that conservation action is not guaranteed but must be consistently encouraged well after listing. In addition to the three sharks already listed, the pelagic thresher (Alopias pelagicus), bigeye thresher (A. superciliosus), common thresher (A. vulpinus), shortfin mako, longfin mako (Isurus paucus), porbeagle, and oceanic whitetip (Carcharhinus longimanus) are considered globally Vulnerable based on IUCN Red List criteria and catch trends (IUCN, 2006) and clearly meet criteria for listing under CMS. In March 2007, the Scientific Council of CMS concluded that 35 species of migratory sharks and rays considered Threatened by IUCN also meet the criteria for listing under CMS. Beyond listing species, CMS provides a critical opportunity to address the conservation needs of oceanic sharks left by gaps in fisheries management. In November 2005, CMS Parties adopted Recommendation 8.16 on migratory sharks that urges Range States to strengthen protection for these species and calls for the development of a global conservation agreement that, among other efforts, seeks to mitigate shark bycatch and identify alternatives to consumptive use (e.g., eco-tourism). This is supported by Resolution 8.5. A workshop planned for December 2007 will look more closely at options for international

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cooperation in migratory shark conservation under CMS, based on an options paper prepared by the IUCN Shark Specialist Group (IUCN, 2007). Readers are referred to the latter, Fowler (2002), Fowler and Cavanagh (2005), Lack and Sant (2006), and Walker (2004) for more detailed discussions of these and other international instruments and domestic management opportunities for shark conservation.

Domestic management action Most pelagic sharks move in and out of the exclusive economic zone (EEZ, waters out to 200 miles from shore) of Range States. Although effective management of fisheries taking pelagic sharks will require multinational cooperation throughout their range, most regulations are implemented at the national level by domestic fisheries agencies. These regulations can be applied to fisheries taking pelagic sharks in domestic waters, as well as wherever their flagged vessels fish. Domestic management does not have to await international action: some measures can be implemented as soon as the conservation needs of pelagic sharks are acknowledged. In addition, strong domestic management can provide guidance and leadership for regional efforts within the RFMOs. The taking of pelagic sharks is largely unregulated in most territorial waters of the world, with the majority of the major shark-fishing nations lacking any management for these species (see Fowler et al., 2005). But in the Northwest Atlantic and Oceania, pelagic shark populations have been subject to domestic management: Prior to 1998, only 4 of the 113 shark-fishing nations – Australia, Canada, New Zealand, and the United States – had implemented comprehensive management plans for some of their fisheries taking pelagic sharks (Camhi et al., 1998; Table 34.5). Other than Papua New Guinea and South Africa, they remain the only nations to have done so. Shark finning is prohibited in all waters of the United States and for all its fishing vessels. In the Atlantic, where pelagic sharks are taken mainly as bycatch on longlines targeting tunas and swordfish, the United States has implemented management since 1993. Measures include permits, trip limits, catch quotas (273 t dressed weight for blue, 92 t for porbeagle, and 488 t for other species combined), and recreational bag (one shark per vessel) and size limits, and prohibition on the catch of white, longfin mako, and bigeye thresher sharks (Branstetter, 1999; www.nmfs.noaa.gov/sfa/hms/hmsdocument_files/sharks.htm). A US proposal to prohibit the take of Atlantic porbeagles is pending, with a decision expected in early 2008. Management in the US Pacific for pelagic sharks is limited to “harvest guidelines” (not a quota) for the common thresher and shortfin mako, and protection for the white shark (www.pcouncil.org/pfmcfacts.html; Cailliet and Camhi, 2005). In the North Pacific, the taking of salmon sharks (Lamna nasus) is prohibited in Alaska state waters, allowed as bycatch in federal waters, and subject to an angling bag limit of two sharks per year. In US western Pacific waters, the fishery management plan covers nine pelagic sharks but imposes no management or catch limits for them (Dalzell et al., 2008). Porbeagle, blue, and shortfin mako sharks have been exploited in Canada’s Atlantic waters since the 1960s and first came under management in 1995. Despite being subject to one of the most comprehensive shark assessments ever (Campana et al., 2008) and years of management, the mature porbeagle population has been fished down to about 10% of

2004 elasmobranch landings (t)

Indonesia India Spain Taiwan Province of China

108,944 79,825 51,260 43,797

Mexico Argentina United States Thailand Pakistan Malaysia Japan

37,540 32,039 30,732 27,646 27,363 25,053 23,475

France Brazil Sri Lanka Iran New Zealand United Kingdom Nigeria Portugal Yemen Korea, Republic of Canada Australia

21,799 20,041 19,510 18,318 16,647 16,066 13,560 12,765 12,750 12,265 11,841 11,459

South Africa Ecuador Papua New Guinea

3,716 1,226 ?

Finning banb

Licenses/ limited entry

Commercial quotas

Size limits

Recreational limitsc

Other measuresd
















Stock assessment for bigeye and pelagic threshers; shark management working group; NPOA Gear restrictions; white shark protection; NPOA





B, M

Protected species; NPOA NPOA drafted Ban on drift nets; NPOA Shark working group to oversee data collection; NPOA Gear restrictions





Blue, mako, porbeagle

Blue, mako, porbeagle

B, M

White shark protection










Bycatch limit

C B, M








Bycatch limit

1 shark/day







NPOA White shark protection; Bycatch Code of Practice, gear restrictions, NPOA White shark protection NPOA Gear restrictions; closed areas





Major shark-fishing nation defined as reporting ⬎10,000 t of elasmobranch landings to FAO in 2004. No nation to date has implemented management for the pelagic stingray. Spain, France, United Kingdom, and Portugal fall under the European Union’s shark finning ban. c B: bag limit; C: catch-and-release only; M: minimum size; limits may vary by fishery. d NPOA: National Plan of Action for Sharks has been adopted; for details see Cavanagh et al. (2008). a

b

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Nation

434

Table 34.5 Summary of known management measures for pelagic sharks by major shark-fishing nations as well as others that have implemented relevant management beyond finning bans (for details on finning bans see Table 34.1).a

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its virgin size (DFO, 2002). Continually reducing the annual quota (185 t in 2006 for both targeted and incidental catch) has helped to stabilize the population (Government of Canada, 2007), but at current levels of exploitation porbeagles will not recover to sustainable levels until the 22nd century or later (DFO, 2005). The directed fishery for blue sharks is subject to precautionary allocations (250 t) rather than a restrictive quota, while shortfin mako and other sharks may only be taken as bycatch and may not exceed 50% of the total weight of the directed shark catch onboard (DFO, 2002). Off Canada’s Pacific Coast, blue sharks and pelagic species are only taken incidentally. This bycatch is well documented by observers, but no catch limits have been implemented (Government of Canada, 2007). Finning was banned in all Canadian waters in 1994. Sharks are taken in more than 70 of Australia’s fisheries, of which 7 target sharks (Rose and Shark Advisory Group, 2001). Pelagic sharks, however, are caught in the largest numbers as bycatch in the eastern and the southern/western tuna and billfish fisheries. These pelagic fisheries are among the best researched in the world, and Australia is one of the few countries to have produced both a Shark Assessment Report and National Plan of Action for Sharks (NPOA-Sharks), and domestic regulation of bycatch in its tuna fisheries is increasing (Stevens et al., 2005). Beyond the protection of the white shark in all Australian waters, there are few speciesspecific measures for sharks taken as bycatch (Shark Advisory Group and Lack, 2004). Commonwealth fisheries (3–200 miles) are subject to federal regulations that include fishing permits, trip limits, and finning prohibitions. Australia’s Tuna and Billfish Bycatch Action Plan sets a 20-shark bycatch limit, bans finning, and established a bilateral Shark Bycatch Code of Practice with Japan that calls for species-specific recording of both catches and discards and encourages live release (AFMA, 2003). Shark finning is banned in most of Australia. In Commonwealth waters finning is prohibited in tuna longline fisheries and for all sharks taken incidentally. Finning regulations vary in enforcement terms among the six states and two mainland territories, but in most places sharks must be landed with their fins attached. Although finning is not banned in Northern Territory waters, the incidental catch of sharks is not allowed. Blue, porbeagle, and mako sharks are taken in large numbers in New Zealand pelagic longline fisheries targeting southern bluefin and bigeye tunas. Finning in these fisheries is widespread (Stevens et al., 2005), yet despite vocal pressure from some constituencies, no domestic bans on shark finning have been implemented to date. The three pelagic sharks above, however, were put under New Zealand’s Quota Management System (which is similar to an individual quota system) in 2004. In 2007, the white shark received full protection within New Zealand’s waters and from fishing by New Zealand-flagged boats on the high seas. New Zealand is in the process of drafting its National Shark Plan. After 10 years of negotiations, Mexico implemented management for targeted sharks, including blue, thresher, and silky sharks (Carcharhinus falciformis), in May 2007 (NOM029-PESC-2004–2006). The new measures, which build on prior license limitations, include a ban on finning, efforts to address bycatch (e.g., gear restrictions and area closures), improvements in species-level data collection, and establishment of an observer program (Sosa-Nishizaki et al., 2008). Perhaps the world’s most progressive and comprehensive management for oceanic sharks is taking place in Papua New Guinea, which “recognizes longline shark fishing,

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based primarily on oceanic shark species, as a legitimate sustainable fishery if subject to proper management.” Since 2003, its National Shark Longline Management Plan mandates license and gear restrictions, limits the total number of hooks per day, establishes closed areas, sets an annual quota of 2,000 t (dressed weight) including discards, requires logbooks and observer coverage, prohibits transshipments at sea, establishes a national advisory committee, and calls for cooperative research (Anonymous, 2002). If effectively implemented, PNG’s precautionary shark management plan could serve as a model for other fishing nations in the region and around the world. A handful of other fishing nations have imposed much more limited measures for pelagic sharks. Taiwan established a Shark Resources Management Working Group to discuss management and conservation issues in 2001. However, beyond promoting full utilization and fisheries data collection for blue, mako, and silky sharks, no other management is being implemented for oceanic shark species (Taiwan Fisheries Agency, 2006). Malaysia has taken an important first step toward management by producing its National Shark Plan. Yet there is no explicit existing or planned management for sharks in Malaysia other than protection for whale sharks and mandatory catch-and-release for a few species taken by anglers (Ali et al., 1999; Malaysia Department of Fisheries, 2005). The Republic of Korea implemented an observer program for its distant-water tuna fisheries in 2005 (An et al., 2006), which may begin to provide fishery data on their significant pelagic shark bycatch; otherwise there are no other shark management measures in place in Korea (Simpfendorfer et al., 2005). More than most nations, Japan has undertaken extensive research and some assessment of its pelagic shark fisheries (Nakano, 1999; Simpfendorfer et al., 2005). However, no measures to manage the take of pelagic sharks exist, and Japan’s National Shark Plan even condones shark finning in its distant-water fleets, provided it does not pose a problem for the status of the resource (Government of Japan, 2001). There is no management for pelagic sharks by the top three shark-fishing nations of Indonesia, India (Hanfee, 1999), and Spain, nor for Sri Lanka (Joseph, 1999), which together accounted for nearly one-third of the world’s elasmobranch landings in 2004 (FAO, 2007). South Africa is instituting license limitations to reduce, if not to phase out, fisheries directed at pelagic sharks. It has adopted a 10% bycatch limit on pelagic sharks taken incidentally in the longline fishery that, in effect, promotes the release of blue sharks, and a recreational bag limit of one shark per day (C. Smith, personal communication; Japp, 1999). The finning ban, however, allows a 14% fin-to-carcass ratio (dressed weight) for foreign vessels, potentially undermining its effectiveness. Costa Rica’s finning ban mandates the best enforcement method available: landing sharks with their fins attached. The ban, however, is not well enforced and no other protections or management measures exist for any shark species (R. Arauz, personal communication). In addition to the foregoing, a few nations have taken action to protect individual species from direct exploitation (Table 34.2). In 1999, South Africa became the first nation to protect the white shark, which is now among the most protected shark species in the world: It is also protected in Australia, Croatia, the European Union, Malta, Mexico, Namibia, New Zealand, and the United States. Although sometimes targeted for its jaws and teeth, indirect fishing mortality poses a larger threat to this relatively rare and unproductive species. The United States and Canada have both added porbeagle sharks to their respective “species

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of concern” lists, yet both countries still allow targeted fishing for the species. Sweden may be the only nation that has prohibited the catch and landing of porbeagle sharks.

Conclusions It is widely acknowledged that sharks are highly vulnerable to overexploitation and that targeted shark fisheries tend to collapse (Camhi et al., 1998; Musick, 2004). Indeed, their conservative life histories of slow growth and late maturity make them among the most vulnerable species inhabiting the seas (Au et al., 2008; Cortés, 2008; Smith et al., 2008). Yet sharks, particularly pelagic sharks, remain a low priority for fishery managers. Despite a wide array of management tools at our disposal – at all levels of governance – large gaps remain in our management of fisheries that incidentally catch or intentionally target oceanic sharks. Repeated calls for improved species-specific catch and mortality data collection have yet to be widely fulfilled. Lack of data, however, should not be used as an excuse for management inaction. All oceanic sharks are listed under the Law of the Sea (UNCLOS Annex 1) and therefore should be afforded precautionary management under international law. The current state of shark fisheries data precludes comprehensive population assessments and models in most cases (Camhi et al., 2008). However, where catch-rate trends have been assessed for oceanic sharks, almost 80% are declining and none are increasing (Camhi, 2008). Some populations have been depleted by as much as 80–90% (Baum and Myers, 2004; Campana et al., 2008; Hueter and Simpfendorfer, 2008). Despite these severe declines, management action for pelagic elasmobranchs lags far behind management for the more economically valuable target teleosts taken in the same fisheries. Long-term, effective conservation of pelagic sharks requires elevated priority of these species in existing forums and quite possibly institutional changes and new international management instruments. At current fishing rates, however, vulnerable pelagic shark populations cannot sustain the wait for these changes. In order to stem population declines and minimize recovery periods, immediate, restrictive action is needed. Existing scientific advice can no longer be ignored and precautionary action must be taken in its absence. Where political will exists, shark fisheries management has progressed: Finning bans have proliferated at a remarkable pace in this century among fishing nations as well as RFMOs. If effectively implemented, finning bans can reduce waste and shark-fishing mortality and serve as a significant step in the right direction, especially when no other shark safeguards are on the horizon. Still, such measures are not a panacea and “full utilization” should not be equated with effective management: We can still fully utilize sharks to the point of endangerment. Meaningful, science-based limits on fishing are needed, in conjunction with finning bans, to prevent irreparable depletion of shark populations and to ensure that shark fisheries operate in a sustainable manner. The state of fisheries management for the 12 oceanic elasmobranchs addressed in this volume can be summarized as follows. One species – the white shark – is listed on CITES, CMS, and the Barcelona Convention, and has received protected species status by a handful of fishing nations and the European Union. Finning bans, some flawed and lenient, have been implemented in most waters. There is no international agreement or

438

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regional management body that specifically addresses the management needs of sharks. No international catch limits on sharks have been adopted, nor have regional mortality caps been officially recommended for any pelagic shark fishery. Only about five or six nations have taken the unilateral step to implement catch quotas for pelagic sharks based on landings or assessments. Even for porbeagle of the North Atlantic – the population with the best data and the only one subject to a comprehensive population assessment – fisheries managers in Canada and the United States have established catch limits but stopped short of full protection for this severely depleted species. Nowhere, to date, has the management of fisheries taking pelagic sharks, as either targeted or incidental catch, been proven to be effective in preventing overfishing. Given the depleted global status of oceanic sharks and declining catch trends (IUCN, 2006; Maguire et al., 2006; Camhi, 2008), it may be disingenuous to be advocating for “precautionary” management: It is simply too late for that. For many populations, such as the North Atlantic porbeagle, aggressive, restorative management is urgently needed.

Recommendations Best practices to improve the overall effectiveness of RFMOs have been well articulated by Willock and Lack (2006) and are relevant to fisheries taking pelagic elasmobranchs. More specifically, the following recommendations are needed to improve the conservation status of oceanic sharks: Fishing nations that have not already done so should ratify or accede to UNCLOS, the • UNFSA, and other relevant treaties. Fishing nations should take the necessary steps to become members, or at least cooper• ating nonmembers, of relevant RFMOs. nations and RFMOs should draft and implement their Shark Plans in accord• Fishing ance with the IPOA-Sharks and include binding, science-based management measures

• • • • •

specific to pelagic sharks (Cavanagh et al., 2008). Nations that share pelagic shark populations should adopt bilateral fishery management agreements and promote complementary measures for adjacent international waters. Nations and RFMOs should eliminate overcapacity and associated subsidies for pelagic shark fisheries. Nations and RFMOs should improve monitoring and enforcement in pelagic shark fisheries through collection of species-specific data on landings and discards (facilitated by training where needed), observer coverage, electronic logbooks, and increased inspection. Nations and RFMOs that have not already done so should adopt finning bans that require sharks to be landed with fins attached. Existing finning bans should be amended to require that sharks be landed with their fins attached, and in the meantime ensure that fin-to-carcass ratios not exceed 5% of dressed weight or 2% of whole weight. Nations and RFMOs should implement science-based precautionary catch limits on targeted pelagic shark populations now until data allow comprehensive population assessments to fine-tune allowable catches.

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and RFMOs should immediately halt targeted fishing for pelagic sharks con• Nations sidered endangered or critically endangered by the IUCN (e.g., North Atlantic porbea-

• • • • •

gle sharks). CITES Parties should work to ensure that advice from its Animals Committee with regard to sharks is heeded and that CITES’ shark efforts continue. Fishing nations should develop and promote options for new international and global conservation agreements for migratory sharks. CMS Parties and relevant fishing nations should work to ensure that shark listings are followed up with regional management plans, as intended. RFMOs should work cooperatively with CITES and CMS to provide comprehensive conservation programs that address both fishing and trade of pelagic sharks. Nations and RFMOs should elevate the priority of research into shark bycatch-reduction methods and related gear modifications.

Significant progress toward pelagic shark assessment and conservation has been made since the early 1990s. Yet, on balance, the depletion of the world’s oceanic sharks is rapidly outpacing the implementation of management measures. On one hand, a landmark IPOA-Sharks has been endorsed by most of the world’s fishing nations, examination of pelagic shark fisheries has been enhanced, and international fisheries and wildlife organizations have begun to turn their attention to sharks. On the other hand, there are still no international limits and few domestic restrictions on pelagic shark catch. Specific data and robust assessments are still lacking, but what we do know about the status and vulnerability of these populations is cause for concern. Without active management, shark fisheries and populations tend to quickly collapse, yet can take decades to rebuild. Therefore, as a matter of priority, current efforts in data collection, species listings, and other means of highlighting concern for pelagic sharks must be followed up with meaningful restrictions on fishing. The management tools for ensuring sustainable shark fisheries are already available at domestic, regional, and international levels; what is lacking is the public pressure and political will to use them. The longer we wait, the longer it will take to recover depleted populations of oceanic sharks, as well as the fisheries and ecosystems they support.

Acknowledgments The authors wish to thank Randall Arauz, Ramon Bonfil Claudine Gibson, Kelly Malish, Herman Oosthuizen, Craig Smith, Sarah Valenti, and Susie Watts for providing valuable information and helpful comments on the manuscript.

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Fowler, S. L., Raymakers, C. and Grimm, U. (2004) Trade in and conservation of two shark species, porbeagle (Lamna nasus) and spiny dogfish (Squalus acanthias). Federal Agency for Nature Conservation, Bonn, Germany. www.cites.org/common/cop/13/inf/E13i-16.pdf, accessed 20 April 2007. Fowler, S. L., Cavanagh, R. D., Camhi, M., Burgess, G. H., Cailliet, G. M., Fordham, S. V., Simpfendorfer, C. A. and Musick, J. A. (eds.) (2005) Sharks, Rays, and Chimaeras: The Status of the Chondrichthyan Fishes. IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, 461 pp. Gilman, E., Clarke, S., Brothers, N., Alfaro-Shigueto, J., Mandelman, J., Mangel, J., Petersen, S., Piovano, S., Thomson, N., Dalzell, P., Donoso, M., Goren, M. and Werner, T. (2007) Shark Depredation and Unwanted Bycatch in Pelagic Longline Fisheries: Industry Practices and Attitudes, and Shark Avoidance Strategies. Western Pacific Regional Fishery Management Council, Honolulu, HI, 217 pp. GFCM (2005) Recommendation [04-10] by ICCAT concerning the conservation of sharks caught in association with fisheries managed by ICCAT. www.iucn.org/places/medoffice/documentos/ GFCM29.pdf, accessed 20 April 2007. Government of Canada (2007) National Plan of Action for the Conservation and Management of Sharks. Fisheries and Oceans, Ottawa, Ontario, Canada, 31 pp. www.dfo_mpo.gc.ca/misc/npoa_ pan/npoa_sharks-e.htm, accessed 22 September 2007. Government of Japan (2001) Japan’s National Plan of Action for the Conservation and Management of Sharks, 7 pp. www.fao.org/figis/servlet/static?xml⫽ipoa_sharks.xml&dom⫽org&xp_nav⫽3, accessed 28 January 2007. Hanfee, F. (1999) Management of shark fisheries in two Indian coastal states: Tamil Nadu and Kerala. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 316–338. Hareide, N. R., Carlson, J., Clarke, M., Clarke, S., Ellis, J., Fordham, S., Fowler, S., Pinho, M., Raymakers, C., Serena, F., Seret, B. and Polti, S. (2007) European Shark Fisheries: A Preliminary Investigation into Fisheries, Conversion Factors, Trade Products, Markets, and Management Measures. European Elasmobranch Association. Hueter, R. E. and Simpfendorfer, C. A. (2008) Case study: Trends in blue shark abundance in the western North Atlantic as determined by a fishery-independent survey. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. IATTC (2002) Resolution on bycatch. Resolution C-02-05. www.iattc.org/ResolutionsENG.htm, accessed 20 April 2007. IATTC (2005) Resolution on the conservation of sharks caught in association with fisheries in the Eastern Pacific Ocean. Resolution C-05-03. www.iattc.org/ResolutionsActiveENG.htm, accessed 20 April 2007. IATTC (2007) Proposal for a comprehensive assessment of key shark species caught in association with fisheries in the Eastern Pacific Ocean. SAR-8-15. www.iattc.org/PDFFiles2/SAR-815-Shark-research-plan.pdf, accessed 20 April 2007. ICCAT (2004) Recommendation by ICCAT concerning the conservation of sharks caught in association with fisheries managed by ICCAT. BYC 04-10. www.iccat.es/Documents/Recs/compendiopdf-e/2004-10-e.pdf, accessed 20 April 2007. ICES (2006) Report of the Working Group on Elasmobranch Fisheries (WGEF). www.ices.dk/ reports/ACFM/2006/WGEF/WGEF2006.pdf, accessed 20 April 2007. IOTC (2005) Concerning the conservation of sharks caught in association with fisheries managed by IOTC. Resolution 05/05. www.iotc.org/English/resolutions/reso_detail.php?reso⫽39, accessed 20 April 2007.

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IUCN (2003) Shark Finning. Information paper, 3 pp. www.flmnh.ufl.edu/fish/organizations/ssg/ finning.htm, accessed 3 March 2007. IUCN (2006) 2006 IUCN Red List of Threatened Species. www.iucnredlist.org, accessed 20 April 2007. IUCN (2007) Review of Migratory Chondrichthyan Fishes. www.cms.int/bodies/ScC/14th_ scientific_council/pdf/en/ScC14_Doc_14_Review_Chondrichthyan_Fishes_Eonly.pdf, accessed 20 April 2007. Japp, D. W. (1999) Management of elasmobranch fisheries of South Africa. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 199–217. Joseph, L. (1999) Management of shark fisheries in Sri Lanka. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 339–366. Lack, M. and Sant, G. (2006) Confronting Shark Conservation Head On! TRAFFIC International, Cambridge, UK, 29 pp. Maguire, J.-J., Sissenwine, M., Csirke, J., Grainger, R. and Garcia, S. (2006) The State of World Highly Migratory, Straddling and Other High Seas Fishery Resources and Associated Species. FAO Fisheries Technical Paper No. 495. FAO, Rome, Italy, 96 pp. Malaysia Department of Fisheries (2005) Malaysia National Plan of Action for the Conservation and Management of Shark (Draft). Department of Fisheries, Kuala Lumpur, Malaysia, 57 pp. www.fao.org/figis/servlet/static?xml⫽ipoa_sharks.xml&dom⫽org&xp_nav⫽3, accessed 28 January 2007. Musick, J. A. (2004) Management of sharks and their relatives (Elasmobranchii). In: Elasmobranch Fisheries Management Techniques (eds. J. Musick and R. Bonfil). Asia Pacific Economic Cooperation, Singapore, pp. 1–8. www.flmnh.ufl.edu/fish/organizations/ssg/EFMT/1.pdf, accessed 6 May 2007. Musick, J. A., Burgess, G., Cailliet, G., Camhi, M. and Fordham, S. (2000) Management of sharks and their relatives (Elasmobranchii). Fisheries 25(3), 9–13. Myers, R. A., Baum, J. K., Shepard, T. D., Powers, S. P. and Peterson, C. H. (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850. Nakano, H. (1999) Fishery management of sharks in Japan. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 552–579. Pikitch, E. K., Camhi, M. D. and Babcock, E. A. (2008) Introduction to Sharks of the Open Ocean. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Rose, C. and Shark Advisory Group (2001) Australian Shark Assessment Report. Commonwealth Department of Agriculture, Fisheries and Forestry, Canberra, Australian Capital Territory, Australia, 211 pp. www.daffa.gov.au/fisheries/environment/bycatch/sharkplan, accessed 6 May 2007. Rose, D. A. (1996) An Overview of World Trade in Sharks and Other Cartilaginous Fishes. TRAFFIC International, Cambridge, UK. Shark Advisory Group and Lack, M. (2004) National Plan of Action for the Conservation and Management of Sharks (Shark-plan). Commonwealth Department of Agriculture, Fisheries and Forestry, Canberra, Australian Capital Territory, Australia, 82 pp. www.daffa.gov.au/fisheries/ environment/bycatch/sharkplan, accessed 28 January 2007. Simpfendorfer, C. A., Cavanagh, R. D., Tanaka, S. and Ishihara, H. (2005) Northwest Pacific. In: Sharks, Rays and Chimaeras: The Status of the Chondrichthyan Fishes (eds. S. L. Fowler et al.). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 150–161.

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Small, C. (2005) Regional Fisheries Management Organisations: Their Duties and Performance in Reducing Bycatch of Albatrosses and Other Species. BirdLife International, Cambridge, UK, 103 pp. Sosa-Nishizaki, O., Márquez-Farías, J. F. and Villavicencio-Garayzar, C. (2008) Case study: Pelagic shark fisheries along the west coast of Mexico. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Smith, S. E., Au, D. W. and Show, C. (2008) Intrinsic rates of increase in pelagic elasmobranchs. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Stevens, J. D., Bonfil, R., Dulvy, N. K. and Walker, P. A. (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57, 476–494. Stevens, J. D., Simpfendorfer, C. A. and Francis, M. (2005) Southwest Pacific, Australasia, and Oceania. In: Sharks, Rays and Chimaeras: The Status of the Chondrichthyan Fishes (eds. S. L. Fowler et al.). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 161–172. Taiwan Fisheries Agency (2006) Taiwan’s National Plan of Action for the Conservation and Management of Sharks. Fisheries Agency, Taipei, Taiwan. www.fa.gov.tw/eng/guide/npoasharke .php, accessed 28 January 2007. UNGA (2006) Sustainable fisheries, including through the 1995 Agreement for the Implementation of the Provisions of the United Nations Convention on the Law of the Sea of 10 December 1982 relating to the Conservation and Management of Straddling Fish Stocks and Highly Migratory Fish Stocks, and related instruments. A/RES/58/14 (2003), A/RES/59/25 (2004), A/59/298 (2004) A/RES/60/31 (2005), and A/RES/61/105. www.un.org/depts/los/general_assembly/ general_assembly_resolutions.htm, accessed 18 February 2007. Walker, T. I. (2004) Elasmobranch fisheries management techniques. In: Elasmobranch Fisheries Management Techniques (eds. J. Musick and R. Bonfil). Asia Pacific Economic Cooperation, Singapore, pp. 285–322. Ward, P. and Myers, R. A. (2005) Shifts in open-ocean fish communities coinciding with the commencement of commercial fishing. Ecology 86(4), 835–847. Watson, J. W., Epperly, S. P., Shah, A. K. and Foster, D. G. (2005) Fishing methods to reduce sea turtle mortality associated with pelagic longlines. Canadian Journal of Fisheries and Aquatic Sciences 62, 965–981. WCPFC (2006) Conservation and management measure for sharks in the Western and Central Pacific Oceans. Conservation and Management Measure 2006-05. www.wcpfc.int/decisions .htm, accessed 12 March 2006. Weber, M. L. and Fordham, S. V. (1997) Managing Shark Fisheries: Opportunities for International Conservation. TRAFFIC International and the Center for Marine Conservation, Washington, DC. Willock, A. and Lack, M. (2006) Following the Leader: Learning from Experience and Best Practice in Regional Fisheries Management Organizations. WWF International, Gland, Switzerland and Traffic International, Cambridge, UK, 64 pp. Yokota, K., Kiyota, M. and Minami, H. (2006) Shark catch in pelagic longline fishery: Comparison of circle and tuna hooks. Fisheries Research 81, 337–341.

Chapter 35

The Rise and Fall (Again) of the Porbeagle Shark Population in the Northwest Atlantic Steven E. Campana, Warren Joyce, Linda Marks, Peter Hurley, Lisa J. Natanson, Nancy E. Kohler, Christopher F. Jensen, Joseph J. Mello, Harold L. Pratt Jr., Sigmund Myklevoll and Shelton Harley

Abstract A comprehensive population dynamics analysis of porbeagle shark (Lamna nasus) in the Northwest Atlantic indicates that the population has collapsed for the second time in its 43-year fishing history. The virgin population in the early 1960s supported annual catches of over 9,000 metric tons (t) before the fishery collapsed in 1967. After a partial recovery over the next 25 years, annual catches of 1,000–2,000 t throughout the 1990s appear to have once again driven the population to record-low numbers. Both the size and the age composition of the catch have declined markedly since 1990, with relatively few large sharks left in the population. Commercial catch rates are now only 10–30% of those in the early 1990s. Both Petersen calculations based on tag recaptures and an age- and sexstructured population model suggest that recent biomass is 10–20% of that present in the virgin population. Porbeagle have a low pup production rate and mature considerably after the age at which they first appear in the fishery. In light of the very low numbers of mature females now found in the population, it is unlikely that even the strict quota management that has been implemented will allow the population to rebuild quickly. However, a 75% reduction in fishing mortality, accurate monitoring of catch, effort, and size composition, and area closures to protect mating aggregations have all been put into place to allow population recovery. Key words: porbeagle, Lamna nasus, overfishing, population dynamics, stock abundance.

Introduction The porbeagle shark (Lamna nasus, Lamnidae) is a large, cold-temperate pelagic species that occurs on both sides of the North Atlantic Ocean, as well as in the South Atlantic and South Pacific Oceans. In the Northwest Atlantic, the species range extends from Newfoundland to New Jersey and possibly to South Carolina, but it is most abundant off the eastern coast of Canada between the Gulf of Maine and Newfoundland (Templeman, Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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1963). It is the only large shark species for which a directed commercial fishery exists in Canadian coastal waters (Hurley, 1998). Even though surprisingly little is known of the biology of this species (Aasen, 1963; Francis and Stevens, 2000) and almost nothing of its population dynamics, the porbeagle population in the Northwest Atlantic has often been cited as a clear example of stock collapse in an elasmobranch (Anderson, 1990; Walker, 1998; Stevens et al., 2000). This widely accepted conclusion is based on the detailed catch records of the Norwegian longliners who first arrived in the Northwest Atlantic to fish the virgin (previously unfished) population in 1961. By 1967, the fishery had almost disappeared because of low catch rates and “unprofitable sizes” (Myklevoll, 1989). At the time it was clear that the fishery had suffered an economic collapse. What was not so clear was whether there had been a corresponding population collapse. In recent years, an increasing number of countries have considered legislation to protect endangered elasmobranch populations, highlighted by the Food and Agriculture Organization’s (FAO) International Plan of Action for the Conservation and Management of Sharks, which noted that many of the world’s shark species are severely depleted (FAO, 1998). Numerous authors have documented the low productivity of elasmobranchs compared to teleosts, largely owing to their low fecundity and delayed age at sexual maturation, and have suggested that only a handful of fast-growing, fecund species are able to sustain a fishery (Cortés, 1998; Walker, 1998; Musick, 1999; Stevens, 1999). Because the porbeagle collapse has received such widespread attention, it is important that the fishery collapse and any subsequent recovery be documented and understood. This chapter presents the first complete analysis of the past and present status of porbeagle population dynamics in the Northwest Atlantic. It builds upon a recent population dynamics analysis by Campana et al. (2002b). New to the current analysis are direct estimates of the natural mortality rate, virgin population biomass, and yield per recruit, and a comprehensive ageand sex-structured population model. The analysis concludes with an evaluation of the likelihood of population recovery after a period of unsustainable exploitation.

Fishery and population dynamics The fishery The fishery for porbeagle sharks in the Northwest Atlantic (NAFO areas 3–6) started in 1961 when Norwegian vessels began exploratory fishing on what was then a virgin population. These vessels had previously fished for porbeagle in the Northeast Atlantic, and they were joined by vessels from the Faroe Islands during the next few years. Reported landings in the Northwest Atlantic rose from about 1,900 t in 1961 to over 9,000 t in 1964, and then fell to less than 1,000 t in 1970 (Fig. 35.1). Although the fishery remained unrestricted, landings were less than 500 t until 1989. Reported landings rose to about 2,000 t in 1992 as a result of increased effort by Faroese vessels and the entry of Canadian vessels. Faroese participation was phased out of the directed fishery by 1994, at which time total landings by three Canadian offshore pelagic longline vessels and a number of inshore vessels was about 1,600 t. Since that time, the fishery has been almost exclusively

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8,060 t 4,000 Canada Faroe Islands Norway Other

Catch (t)

3,000

2,000

1,000

0 1960

1970

1980

1990

2000

Year Fig. 35.1 Reported landings (in metric tons) of porbeagle in the Northwest Atlantic by country.

Canadian, with landings declining gradually to 1,066 t in 1998. Landings from 1998 to 2001 were restricted by quota control to below 1,000 t, and further restricted to 250 t beginning in 2003. Detailed landings data were presented in Campana et al. (2002b). The first fishery management plan for any pelagic shark species in Atlantic Canada was implemented in 1994. The plan provided for the collection of catch and effort data through the completion and submission of logbooks, and for collection of sampling data (species, sex, length, weight) for each shark landed through a dockside monitoring program. In 1997, a more comprehensive plan was released to govern the exploitation of all large pelagic shark species through the maintenance of a biologically sustainable resource and a self-reliant fishery. Conservation was not to be compromised and a precautionary approach was to guide decision making. All licenses issued under the plan were to be considered exploratory while scientific information was collected and the sustainability of the resource was evaluated. The management plan of 2000–2001 was the first to be based on the new scientific data and the accompanying analytical stock assessment for porbeagle (Campana et al., 1999). In addition to a reduced quota, the plan restricted access to porbeagle mating grounds off southern Newfoundland. Relying on additional scientific information and an improved stock assessment, the management plan of 2002 reduced allowable catches of porbeagle by a further 70% and eliminated access to the mating grounds (Campana et al., 2001). Further details of the shark management plan and of porbeagle management history are presented in Campana et al. (1999, 2001). Porbeagle sharks are taken almost exclusively by a Canadian directed longline fishery that focuses on largely immature porbeagles on the Scotian Shelf in spring and on larger, primarily mature animals off Newfoundland and the Gulf of St. Lawrence (NF-Gulf) in the fall (Fig. 35.2). Both inshore and offshore fleets fished the Shelf in the spring of

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Inshore fleet (⬍33 m) July–December 1999–2000

Inshore fleet (⬍33 m) January–June 1999–2000

800

6,000 4,000

400

2,000 0

50

75

125

50

175 225 275 Fork length (cm)

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Fork length (cm)

45

45

Metric tons 5 12.5 25 37.5

40

Latitude

0 75

70

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Metric tons 5 12.5 25 37.5

40 70

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55

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40 70

50

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Longitude

Fig. 35.2 Catch location and associated length composition for Canadian inshore (⬍33 m) and offshore (⬎33 m) vessels in spring (January–June) and fall (July–December) of 1999–2000. The size of the symbol is proportional to the size of the catch.

recent years, although the offshore fleet tended to fish near the edge of the continental shelf while the inshore fleet fished well onto the Shelf. Fishing by both fleets was minimal in the summer. In the fall, the small amount of catch taken by the inshore fleet was mainly from the Scotian Shelf, while the much larger offshore catches were made in the Gulf of St. Lawrence, off southern Newfoundland, and on the Grand Banks (Fig. 35.2). Porbeagle bycatch in the Canadian swordfish (Xiphias gladius, Xiphiidae) longline fishery, the Japanese tuna (Thunnus spp., Scombridae) longline fishery, and various inshore fisheries is minimal, seldom exceeding 40 t in recent years (Table 35.1). Though the reported catches of shortfin mako (Isurus oxyrinchus, Lamnidae) and unspecified sharks prior to 1996 were likely to have been mainly porbeagle, the effect on the overall catch trend is minimal. The International Observer Program has maintained 100% coverage of foreign catches in the Canadian zone since 1987, thus ensuring the accuracy of the foreign catches since that time. The recreational fishery for porbeagle sharks is minimal.

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Table 35.1 Landings (t) of porbeagles, sharks reported as makos, and unspecified sharks by fishery from Canadian waters; total allowable catch is for porbeagle only. Year

Directed longline

1991 1992 1993 1994 1995 1996 1997 1998 1999 2000

329 805 912 1,552 1,313 1,024 1,295 1,020 930 888

Swordfish bycatch 0 0 0 9 21 6 6 8 2 2

Tuna bycatch

Other bycatch

Reported as mako

0 0 0 2 0 1 0 0 1 1

0 9 8 18 15 24 40 28 23 8

0 0 4 142 111 67 86 71 64 62

Reported as unspecified shark 185 171 174 121 40 20 43 37 16 13

Total shark

Total allowable catch

514 985 1,098 1,844 1,500 1,142 1,470 1,164 1,036 974

– – – – 1,500 1,500 1,000 1,000 1,000 850

210

Median fork length (cm)

200 190 180 170 160 150 140 1960

1970

1980

1990

2000

2010

Year Fig. 35.3 Long-term changes in the median size of porbeagles in the commercial catch by the offshore fleet during September–October on the southern Newfoundland mating grounds. A Loess curve has been fit to the data.

Trends in length and age composition A biological indicator of a high exploitation rate is a long-term decline in fork length in the catch. Because more than 142,000 porbeagle measurements were collated from a variety of sources for this study (Campana et al., 2002b), analyses of trends in median size at age were possible. A plot of median fork length (measured over the curve of the body) against year of collection showed a long-term decline on the NF-Gulf mating ground in early fall (Fig. 35.3). The median lengths for the years prior to 1980 are most representative of the length composition of a lightly fished population. In contrast, 1999 and 2000 were characterized by very low median sizes, indicating the loss of many sharks of mature

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size. There were no consistent long-term trends in size composition on the Scotian Shelf, an area dominated by smaller, primarily immature porbeagles. Age determinations are an important component of a population analysis because ages form the basis for both growth and mortality rates. Natanson et al. (2002) presented a validated growth model for Northwest Atlantic porbeagles based on counts of growth bands in vertebral cross sections. The accuracy of the age interpretations was validated to an age of 11 years using known-age and tetracycline-injected recaptures (Natanson et al., 2002), and subsequently to an age of 26 years using bomb radiocarbon dating (Campana et al., 2002a). Although there was evidence of sexually dimorphic growth after the onset of sexual maturity, the difference in size at age was small. Therefore, a sex-combined growth curve was used to convert catch at length to catch at age using the approach described in Campana et al. (2002b). The age composition of past and present landings shows evidence of increased exploitation. In recent years, the age of full recruitment to the fishery has dropped to only 2–3 years in all areas. Prior to 1993, full recruitment occurred at 6–7 years. Prior to 1991, the most abundant age class off southern Newfoundland in the fall was 10–15 years, consistent with the use of this area as a mating ground by a lightly fished population. In contrast, porbeagle less than 3 years were the most abundant age classes in the NF-Gulf catch of 1998–2000.

Commercial catch rates The overall trend in catch rate was analyzed using a linear model with subarea, month, fishing vessel, and year as factors (Campana et al., 2002b). Calculations were based on directed longline catches, which account for virtually all historical catches. The standardized catch rate of mature porbeagles increased significantly between 1989 and 1992, but declined sharply afterward as effort increased and the abundance of the large sharks declined (Fig. 35.4). The 2000 point is the second lowest in the time-series, and is 10% of the 1992 value. The standardized catch-rate model for immature porbeagles was also highly significant, and also showed a significant decline since the early 1990s (Fig. 35.4). The 2000 point is about 30% of the 1991 point. However, the catch rate has remained roughly stable since 1996 (ignoring the 1997 value, which is also anomalous in the mature catch-rate series), consistent with the fleet-specific catch rates (Campana et al., 2001). Overall, these catch rates suggest a monotonic and disturbing decline in the abundance of mature sharks, with a low but stable rate for immature sharks.

Estimation of rates of natural and total mortality Trends in ln-transformed catch at age (catch curves) are shown in Fig. 35.5. The upper three panels show the catch curves of the 1961 (virgin) population, while the remainder show the catch curves for each of 3 recent years. Total instantaneous mortality rates (Z) based on the slope of the descending limb of the catch curve indicate that recent mortality rates have usually been higher than those of 1961. However, the exact mortality rate in recent years may be underestimated by the reduced abundance of young sharks. This effect is shown by a much-reduced ascending limb to the catch curve, indicating an

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0.010

Mature sharks/hook

0.008

0.006

0.004

0.002

0.000 1989

1991

1989

1991

1993

1995

1997

1999

Immature sharks/hook

0.18

0.12

0.06

0.00 1993

1995

1997

1999

Fig. 35.4 Standardized catch rate (number per hook) of sexually mature (⬎200 cm fork length) and immature (⬍200 cm) porbeagles. Factors in the analysis included year, month, area, and vessel. Error bars are 95% confidence intervals.

increasingly young age at recruitment to the fishery, which probably explains the apparently low total mortality rate of mature females in the recent NF-Gulf fishery. The estimates of Z from the catch curves for the virgin 1961 population are also estimates of the instantaneous rate of natural mortality (M). Campana et al. (1999) estimated M as 0.1 based on preliminary catch curves. Based on the refined catch curves presented here, M for maturing males on the Shelf indeed appears to be around 0.1 (Fig. 35.5). However, it appeared to be slightly higher (0.15) for fully mature males on the NF mating grounds. M could not be estimated for immature females in 1961, but M for mature females on the mating grounds was estimated as 0.20. There is no reason to expect sex-specific differences in M prior to sexual maturity. Therefore, M was estimated for the combined length frequencies on the Shelf between

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4

Z 16–30 ⫽ 0.15

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Z 3–8 ⫽ 0.27

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⫺1

0

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Age

Fig. 35.5 Catch curves (ln-transformed numbers at age) by subarea used to calculate instantaneous mortality rate (Z) over specified age ranges. The 1961 samples are from a virgin population, and thus Z equals the instantaneous natural mortality rate (M). Decomposition of lengths to ages was based on the combined (across sexes) von Bertalanffy growth model except where indicated.

1998 and 2000 for ages before maturity (3–8 years). The mean Z was 0.21. On the basis of exploitation rate estimated from tag returns (see Petersen analysis below, where recent F ~ 0.09), recent M for immature porbeagles would be 0.12. More precise estimates of M could be calculated given direct aging of samples collected in the 1961 fishery. At this point, however, an M of 0.1 for immature porbeagles of both sexes is consistent with the samples from the virgin population and with recent catch curves. M for mature males was also well estimated at 0.15. M for mature females appears to be higher than that of males and, based on the combined growth curve, would

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be around 0.20. An increased natural mortality in mature animals, particularly females, is consistent with both the observed age composition and life-history theory (Roff, 1984), since mortality would be expected to increase in females carrying large embryos over an extended gestation period. Nevertheless, it appears that this is the first demonstration of this effect in sharks, probably because of the scarcity of reliable age determinations.

Recent mortality rates based on Paloheimo Z’s Total instantaneous mortality rate (Z) in the most recent years was estimated through use of Paloheimo Z’s, based on the reduction in catch at age along a cohort between adjacent years (Ricker, 1975). Details of the porbeagle calculation are presented in Campana et al. (2002b). All five of the mortality estimates ranged between 0.27 and 0.37, with a mean of 0.32. The Z estimates for mature porbeagle on the NF mating grounds were not significantly different from those for immature porbeagle on the Shelf. With a mean Z ⫽ 0.32 for ages 3–9 on the Shelf, and given an immature M ⫽ 0.10 (as calculated earlier), recent fishing mortality on immature Shelf porbeagles would be 0.22. This estimate would be slightly inflated if older but immature females were less available on the Shelf in the spring. In the NF-Gulf area in fall, mean Z for ages 9–13 was estimated as 0.33. Assuming an M ⫽ 0.15 intermediate to that of immature and mature sharks, fishing mortality (F) would be estimated at 0.18.

Petersen calculations of abundance and exploitation rate The biomass of both the virgin porbeagle population of the 1960s and that of the fished population in the 1990s was estimated through Petersen analysis of tag recaptures. Three independent and unpublished tag–recapture studies carried out by the Norwegians (1960s), the United States (1990s), and Canadians (1990s) were used. To optimize estimation rigor, the exploitation rate calculations were restricted to the Canadian and US tagging of age 0 and age 1 sharks (⬍125 cm fork length) between 1993 and 1997. The number of tags applied to these young sharks since 1993 was 1,177, of which 86 were subsequently recaptured. Full details of the biomass calculations (which are calculated for the year of tagging) are shown in Campana et al. (1999), while the exploitation rate calculations (calculated for the year of recapture) are shown in Campana et al. (2002b). The independent US and Canadian tagging studies provided similar estimates of population biomass between 1994 and 1997. These population estimates were about 15–20% of the size of the virgin population tagged by the Norwegians (Fig. 35.6). However, the fact that many large sharks were tagged in the 1960s, but not in the 1990s, makes the population biomass comparison between recent and historic times somewhat tenuous. The recent exploitation rate of the fished population in the 1990s was also estimated through Petersen analysis of tag recaptures, and because these rates are relatively insensitive to the assumptions required of biomass calculations, they are reasonably robust. The unadjusted exploitation rate ranged between 4% and 12%, with a mean of 8%. No trend was apparent across recent years, and the independent US and Canadian tagging studies yielded similar estimates of exploitation rate since 1994. When adjusted for age-specific selectivity (Campana et al., 2002b), the exploitation rate was estimated to lie between 5% and 20%, with a mean of about 11% (Fig. 35.6).

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160,000 140,000

Biomass (t)

120,000 100,000 80,000 60,000 40,000 20,000 0 1960

1970

1980 1990 Year of tagging

2000

(a)

Exploitation rate (%)

0.20

0.16

0.12 Mean 0.08

0.04 1993 1994 1995 1996 1997 1998 1999 2000 2001 Recapture year (b) Fig. 35.6 Estimates of population biomass (a) and fishing mortality (F) (b) based on Petersen analysis of tag recaptures from Canadian, American, and Norwegian tagging studies. Only years with more than four recaptures from a given tagging year are shown in the biomass plot, and years with more than three recaptures for the exploitation plot. The calculations of exploitation rate were restricted to sharks tagged at fork lengths ⬍125 cm in the Canadian and American studies, and thus are most applicable to the spring fishery on the Scotian Shelf. Exploitation rates have been divided by age-specific selectivity to calculate the fully recruited exploitation rate.

Yield per recruit Yield per recruit was calculated on the basis of a fitted growth model (Natanson et al., 2002), an empirical length–weight relationship (Campana et al., 1999), the estimates of immature and mature female natural mortality determined from the catch curve analysis (Fig. 35.5), and an area-specific selectivity curve (Campana et al., 2002b). The estimated F0.1 and yield values were not unduly affected by the selection of natural mortality schedules, although the choice of selectivity vectors was quite influential. Yield in the NF-Gulf

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fishery was estimated to be higher (18.1 kg per recruit), but at a lower F0.1 (0.14), than that on the Shelf (15.4 kg per recruit at F0.1 ⫽ 0.20). Using a combined selectivity vector (effort-weighted 2:1 for Shelf:NF-Gulf), F0.1 was estimated at 0.18 with a yield of 16.7 kg per recruit. Because the age of first capture occurs well before the age of sexual maturity, spawning stock numbers and population biomass would both be expected to be susceptible to even modest fishing mortalities. For example, fishing at F0.1 would be expected to reduce the number of mature females to 18% of their original numbers, and to reduce population biomass to 40% of its original value. Such a sharp decline in the predicted size of the spawning population resembles the decline in the observed catch rate of sexually mature porbeagle (Fig. 35.4). Campana et al. (1999) suggested that an F0.1 yield would not be sustainable unless the F on the mature population was considerably less than F0.1. As documented in the life table analysis in Campana et al. (2002b), it is now clear that F0.1 is not sustainable for porbeagle sharks.

Age- and sex-structured population model A forward-projecting, age- and sex-structured population dynamics model was developed for the Northwest Atlantic porbeagle to estimate current population status relative to that of earlier years. The model was fit to available catch at length and catch per unit effort data between 1961 and 2000, using the growth model, natural mortality rates, maturity ogives, fecundity, and area–season stratification described earlier. The steepness of the Beverton–Holt spawner-recruit model was defined a priori as 0.37 on the basis of the welldefined reproductive parameters of porbeagle (Jensen et al., 2002). The base model assumed a combined-sex growth curve, a higher M in the first year of life, an increased M at the onset of sexual maturity, and a fixed selectivity. Model output included time-trends in biomass, female spawner numbers, and area-specific selectivity curves. AD Model Builder (Otter Research Ltd., Sidney, British Columbia, Canada) was used to prepare the model and fit the likelihood functions. Estimates of both total biomass and spawning stock numbers declined sharply after the onset of the 1961 fishery, increasing slightly through the 1970s and 1980s, then declining once more to a record-low level (Fig. 35.7). Biomass in 2001 was estimated as 11% of the virgin biomass, and fully recruited fishing mortality in 2000 was estimated as 0.26 (Table 35.2). The time-series of fishing mortality indicates that F has been very high since the mid-1990s (Fig. 35.8). Of the four alternative runs considered, none resulted in more optimistic views of recent population status than the base run. The biological reference points predicted by the model were similar in all runs: Maximum sustainable yield (MSY) was estimated to be about 1,000 t at an FMSY of 0.04– 0.05 (Table 35.2).

Discussion All of the indicators examined in the population dynamics analysis of the Northwest Atlantic porbeagle suggest that the population has collapsed for a second time in its

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Spawners

60

40

40

20

20

10

10

Biomass

8

8

6

6

4 1961

Total biomass (000s t)

Female spawner numbers (000s)

60

4 1971

1981

1991

2001

Fig. 35.7 Time trends in porbeagle biomass and female spawner abundance from the base run of the age- and sex-structured population model.

0.8

F

0.6

0.4

0.2

0.0 1961

1971

1981

1991

2001

Fig. 35.8 Time trends in porbeagle fishing mortality (F) from the base run of the age- and sex-structured population model.

43-year fishing history. Average catches of about 4,500 t/year in the early 1960s resulted in a fishery that collapsed after only 6 years and that did not fully recover over the next 25 years. Nevertheless, the fishery appeared sustainable during the 1970s and 1980s, when landings averaged 350 t annually. However, annual catches of 1,000–2,000 t throughout the 1990s appear to have once again impacted the population, driving it to record-low population numbers. Both the size and the age composition of the catch have declined, and

Table 35.2 Output of five realizations of an age- and sex-structured population model for Northwest Atlantic porbeagle.* Run

Female spawners 1961 63,694 64,710 69,186 69,664 100,979

6,075 7,500 2,612 2,934 13,847

2001/1961 0.10 0.12 0.04 0.04 0.14

Exploitation rates in 2000

1961

2001

2001/1961

Age 2

Age 5

Age 8

38,967 39,589 42,327 42,619 44,317

4,409 4,991 1,572 1,928 7,695

0.11 0.13 0.04 0.05 0.17

0.16 0.14 0.41 0.35 0.14

0.25 0.22 0.64 0.52 0.21

0.26 0.23 0.80 0.65 0.26

Base: M increases at maturity, fixed selectivity, combined growth curve. Run 2: As above but with no recruitment deviates. Run 3: Estimating selectivity and recruitment deviates. Run 4: Estimating selectivity without recruitment deviates. Run 5: Estimating selectivity and recruitment deviates with no increased mortality. * B: biomass; B0: virgin biomass; F: fishing mortality; MSY: maximum sustainable yield.

B0 (t)

FMSY

MSY (t)

MSY/B0

38,967 39,589 42,327 42,619 44,317

0.046 0.046 0.047 0.047 0.063

1,069 1,086 1,138 1,143 1,079

0.027 0.027 0.027 0.027 0.024

BMSY (t) 24,402 24,791 26,362 26,519 21,275

B2001/BMSY

0.18 0.20 0.06 0.07 0.36

The Rise and Fall (Again) of the Porbeagle Shark

Base Run 2 Run 3 Run 4 Run 5

2001

Total biomass (t)

457

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Fishing mortality

0.30

0.20

0.10

Zero growth MSY

0.00 Model

Paloheimo

Tagging

Fig. 35.9 Summary of recent fishing mortality (F) estimates derived from independent analyses. Estimates are drawn from analysis of the years 1994–2000 (tagging), 1998–2000 (Paloheimo Z’s), and 2000 (population model). Error bars indicate the approximate range of uncertainty based on multiple estimates. All estimates of recent F are above a level that would allow population recovery (MSY) or maintain current population size (zero growth).

relatively few large sharks are left in the population. Catch rates are now 10–30% of those in the early 1990s. Petersen calculations based on tag recaptures and an ageand sex-structured population model show that recent biomass is only 10–20% of that present in the virgin population. With such a coherent picture of population decline in the face of modest catches, it is clear that the porbeagle population is very susceptible to overexploitation. Life table analysis has indicated that the intrinsic rate of population growth (r) in the unfished porbeagle population varies between 0.05 and 0.07 (Campana et al., 2002b). Such values are very low compared to those of most fishes (Myers et al., 1999), and indicate that the porbeagle population is intrinsically unproductive and slow to recover from stock depletion. Presumably this is because porbeagle produce few offspring and mature at a late age compared with the age of first capture. The current analysis confirms the unsustainability of fishing at F0.1 ⫽ 0.18 for porbeagle, and indicates that a fishing mortality above 0.08 will cause the population to decline. A fishing mortality of 0.04 corresponds to the MSY, and fishing at or below this rate is required if the population is to be allowed to recover. Several independent estimates of recent fishing mortality suggest that recent catches averaging 1,000 t/year have resulted in an unsustainable F of about 0.20 (Fig. 35.9). An annual catch of 200–250 t would correspond to fishing at MSY and would allow population recovery. Many shark species are unproductive compared to teleosts (Musick, 1999). However, with the production of only four pups per year, porbeagle are among the least fecund of the shark species (Aasen, 1963; Francis and Stevens, 2000; Jensen et al., 2002). It is more difficult to compare published natural mortality rates among shark species, since most published estimates have used the predictive models of Hoenig (1983), Pauly (1980),

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and Peterson and Wroblewski (1984) to estimate M, rather than direct measurements as are reported here, owing to lack of data. Nevertheless, porbeagle appear to have a somewhat lower M (⫽0.1) than other shark species, which have been reported to have an M of 0.1–0.6 (Cortés, 1998, 1999; Stevens, 1999). Low values of M are normally associated with low productivity. Fishing quotas based on “conservative” strategies such as F0.1 are commonly used to minimize the probability of either recruitment or growth overfishing in teleost fishes (Mace, 1994). Reporting results that would be viewed with skepticism in a teleost fishery, Rago et al. (1998) calculated that Fmax exceeded the fishing mortality at which population replacement of spiny dogfish (Squalus acanthias, Squalidae) could occur. The implications of our calculations extend beyond those of Rago et al. (1998), demonstrating that even the more conservative F0.1 fishing target is anything but conservative for porbeagle shark, and will eventually lead to stock collapse. Similar conclusions have been reached qualitatively for a wide range of low-productivity shark species, many of which appear incapable of supporting more than a nominal fishing mortality (Cortés, 1998, 1999; Walker, 1998; Musick, 1999; Simpfendorfer, 1999; Stevens, 1999). The inherent vulnerability of sharks and other elasmobranchs to overfishing and stock collapse was recently highlighted in an American Fisheries Society policy statement, which noted that most elasmobranch populations decline more rapidly and recover less quickly than do other fish populations (Musick et al., 2000). Despite obvious indicators of overexploitation, there are some key differences between the current porbeagle fishery and the fishery that was present prior to the 1967 collapse, which suggest that sustainability may yet be possible. More than 80% of the recent annual catch has been taken on the Scotian Shelf in the spring, at a time when availability is largely limited to immature sharks. A fishery that preferentially targets immature sharks is very different than that in the 1960s prior to the fishery collapse, when the fishery focused on aggregations of mature (and possibly mating) sharks in the fall off southern Newfoundland. Fishing mortality is now low and strictly regulated, with minimal bycatch in other fisheries. In addition, the fishing industry provides accurate catch and effort data, and measures each shark individually, thus facilitating population monitoring. Management measures to restrict or eliminate the catch of mature females through closed areas are recent innovations. Finally, and perhaps most importantly, the current porbeagle fishing industry in the Northwest Atlantic is highly motivated to conserve the population, and has assisted in its scientific study. While it remains to be seen if the porbeagle population can be fished sustainably, the necessary elements for a sustainable fishery appear to be in place.

Acknowledgments We thank Clearwater Fine Foods, Karlsen Shipping, and the Atlantic Shark Association for providing access to their fishing vessels and unpublished data in support of the porbeagle research program. We also thank Enric Cortés for assistance with the life table analysis, Jerry Black, Mark Fowler, Bob Mohn, and Steve Smith for analytical advice, and the BIO Assessment Working Group for their critical review and advice.

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References Aasen, O. (1963) Length and growth of the porbeagle (Lamna nasus) in the North West Atlantic. Report on Norwegian Fishery and Marine Investigations 13, 20–37. Anderson, E. D. (1990) Fishery Models As Applied to Elasmobranch Fisheries. NOAA Technical Report NMFS 90. NOAA/NMFS, Silver Spring, MD, pp. 473–484. Campana, S., Marks, L., Joyce, W., Hurley, P., Showell, M. and Kulka, D. (1999) An Analytical Assessment of the Porbeagle Shark (Lamna nasus) Population in the Northwest Atlantic. Document No. 99/158. Canadian Science Advisory Secretariat, Fisheries and Oceans, Ottawa, Ontario, Canada, 57 pp. Campana, S., Joyce, W., Marks, L. and Harley, S. (2001) Analytical Assessment of the Porbeagle Shark (Lamna nasus) Population in the Northwest Atlantic, with Estimates of Long-Term Sustainable Yield. Document No. 2001/067. Canadian Science Advisory Secretariat, Fisheries and Oceans, Ottawa, Ontario, Canada, 59 pp. Campana, S. E., Natanson, L. J. and Myklevoll, S. (2002a) Bomb dating and age determination of large pelagic sharks. Canadian Journal of Fisheries and Aquatic Sciences 59, 450–455. Campana, S. E., Joyce, W., Marks, L., Natanson, L. J., Kohler, N. E., Jensen, C. F., Mello, J. J., Pratt Jr., H. L. and Myklevoll, S. (2002b) Population dynamics of the porbeagle in the Northwest Atlantic Ocean. North American Journal of Fisheries Management 22, 106–121. Cortés, E. (1998) Demographic analysis as an aid in shark stock assessment and management. Fisheries Research 39, 199–208. Cortés, E. (1999) A stochastic stage-based population model of the sandbar shark in the western North Atlantic. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 115–136. FAO (1998) International Plan of Action for the Conservation and Management of Sharks. FAO Document FI:CSS/98/3. FAO, Rome, Italy. Francis, M. P. and Stevens, J. D. (2000) Reproduction, embryonic development and growth of the porbeagle shark, Lamna nasus, in the Southwest Pacific Ocean. Fishery Bulletin 98, 41–63. Hoenig, J. M. (1983) Empirical use of longevity data to estimate mortality rates. Fishery Bulletin 81, 898–903. Hurley, P. C. F. (1998) A review of the fishery for pelagic sharks in Atlantic Canada. Fisheries Research 39, 107–113. Jensen, C. F., Natanson, L. J., Pratt, H. L., Kohler, N. E. and Campana, S. E. (2002) The reproductive biology of the porbeagle shark, Lamna nasus, in the western North Atlantic Ocean. Fishery Bulletin 100, 727–738. Mace, P. M. (1994) Relationships between common biological reference points used as thresholds and targets of fisheries management strategies. Canadian Journal of Fisheries and Aquatic Sciences 51, 110–122. Musick, J. A. (1999) Ecology and conservation of long-lived marine animals. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 1–10. Musick, J. A., Burgess, G., Cailliet, G., Camhi, M. and Fordham, S. (2000) Management of sharks and their relatives (Elasmobranchii). Fisheries 25, 9–13. Myers, R. A., Bowen, K. G. and Barrowman, N. J. (1999) Maximum reproductive rate of fish at low population sizes. Canadian Journal of Fisheries and Aquatic Sciences 56, 2404–2419. Myklevoll, S. (1989) Norway’s Porbeagle Fishery. ICES C.M. 1989: H. International Council for the Exploration of the Sea, Copenhagen, Denmark, 16 pp. Natanson, L. J., Mello, J. J. and Campana, S. E. (2002) Validated age and growth of the porbeagle shark, Lamna nasus, in the western North Atlantic Ocean. Fishery Bulletin 100, 266–278.

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Pauly, D. (1980) On the relationships between natural mortality, growth parameters, and mean environmental temperature in 175 fish stocks. Journal du Conseil International pour l’Exploration de la Mer 39, 175–192. Peterson, I. and Wroblewski, J. S. (1984) Mortality rate of fishes in the pelagic ecosystem. Canadian Journal of Fisheries and Aquatic Sciences 41, 1117–1120. Rago, P. J., Sosebee, K. A., Brodziak, J. K. T., Murawski, S. A. and Anderson, E. D. (1998) Implications of recent increases in catches on the dynamics of Northwest Atlantic spiny dogfish (Squalus acanthias). Fisheries Research 39, 165–181. Ricker, W. E. (1975) Computation and Interpretation of Biological Statistics of Fish Populations. Bulletin No. 191. Fisheries Research Board of Canada, Ottawa, Ontario, Canada, 382 pp. Roff, D. A. (1984) The evolution of life history parameters in teleosts. Canadian Journal of Fisheries and Aquatic Sciences 41, 989–1000. Simpfendorfer, C. A. (1999) Demographic analysis of the dusky shark fishery in southwestern Australia. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 149–160. Stevens, J. D. (1999) Variable resistance to fishing pressure in two sharks: The significance of different ecological and life history parameters. In: Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals (ed. J. A. Musick). American Fisheries Society, Bethesda, MD, pp. 11–15. Stevens, J. D., Bonfil, R., Dulvy, N. K. and Walker, P. A. (2000) The effects of fishing on chondrichthyans, and the implications for marine ecosystems. ICES Journal of Marine Science 57, 476–494. Templeman, W. (1963) Distribution of Sharks in the Canadian Atlantic (with Special Reference to Newfoundland Waters). Bulletin No. 140. Fisheries Research Board of Canada, Ottawa, Ontario, Canada, 77 pp. Walker, T. I. (1998) Can shark resources be harvested sustainably? A question revisited with a review of shark fisheries. Marine and Freshwater Research 49, 553–572.

Chapter 36

Methods to Reduce Bycatch Mortality in Longline Fisheries Daniel L. Erickson and Steven A. Berkeley

Abstract Potential methods for reducing bycatch mortality in longline fisheries were examined by two independent studies. Experiments were conducted onboard commercial fishing boats in the Gulf of Mexico (pelagic longlines; 1994–1997) and the Gulf of Alaska (demersal longlines; 1999). Hook timers, instruments that record the moment when fish strike at baited hooks, and motion detectors were used to determine the amount of time that fish spent hooked on longlines. For pelagic longlines, which were often soaked longer than 20 hours, hook-timer data revealed that mortality of pelagic fishes (e.g., swordfish, Xiphias gladius) increased with greater time spent on the longline. This mortality varied by species, ranging from 100% within 12 hours for swordfish to 30% after 12 hours for sharks. Motion-detector data showed that most demersal fish (e.g., Pacific halibut, Hippoglossus stenolepis) struck at baited hooks within 3 hours after longlines were set, even though sets were soaked for up to 9 hours. Results of these experiments suggest that soaking longlines no more than some optimal duration (e.g., significantly less than 20 hours for pelagic longlines) may increase the survival of bycatch species while maintaining the catch of target species. Optimal soaking duration likely varies by fishery. The surest method for reducing bycatch mortality in any fishery, however, is to avoid hooking unwanted bycatch in the first place. One approach is to develop species-selective baits. We provide an example of an artificial bait developed for demersal longline fisheries that caught target species (i.e., Pacific halibut and sablefish, Anoplopoma fimbria) as efficiently as natural bait, while almost eliminating the catch of nontarget species (e.g., squalid sharks and skates). Key words: artificial bait, bycatch mortality, selectivity, bycatch reduction, longline fisheries, Alaska, Gulf of Mexico, halibut, sablefish, tuna, swordfish.

Introduction Shark is the principal “bycatch” species in most pelagic longline fisheries (Joyce, 1999; Matsunaga and Nakano, 1999; Pawson and Vince, 1999). The high level of shark bycatch, Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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coupled with the life-history characteristics of sharks, has resulted in dramatic population declines for many shark populations throughout the world (Camhi, 1999). Although some researchers (e.g., Matsunaga and Nakano, 1999) have suggested that certain pelagic sharks have shown a constant or increasing catch per unit effort (CPUE) over the past two decades, most report declining catch rates for pelagic sharks in the Atlantic, Pacific, Gulf of Mexico, and the Caribbean (e.g., Cailliet et al., 1991; Holts et al., 1998; Cortés, 1999; Cramer, 1999). Regulatory measures (where they exist) designed to reduce shark bycatch mortality in longline and other fisheries include time and area closures, catch quotas, and size limits (see Cailliet et al., 1991). Time and area closures are effective at reducing bycatch only when target and nontarget species segregate spatially, which is generally not the case for the pelagic sharks caught in longline fisheries targeting tunas (Boggs, 1992; Ward et al., 2004). Catch quotas and size limits can be effective for target species, but often result in discarding and subsequent unaccounted mortality of bycatch species in fisheries with no or limited observer coverage, because discards are usually underreported (Pikitch et al., 1988; Gillis et al., 1995; D. L. Erickson, personal observation). Other management approaches are needed to ensure sustainable shark populations. This chapter presents two alternatives for reducing shark bycatch mortality: shorter soaking periods and species-selective baits.

Methods These data were collected during two independent field studies: a pelagic longline experiment conducted in the Gulf of Mexico during 1994–1997 and a demersal longline study that took place in the Gulf of Alaska in 1999. Instrumentation was used during both studies to describe the effects of soaking duration on catch and bycatch mortality. Species selectivity of a new artificial bait was tested in the Alaska trials.

Gulf of Mexico pelagic longline experiment A pelagic longline experiment was conducted between November 1994 and May 1997 in the Gulf of Mexico onboard commercial fishing vessels targeting yellowfin tuna (Thunnus albacares, Scombridae) and occasionally swordfish (Xiphias gladius, Xiphiidae). This work was conducted during regular commercial fishing operations (i.e., vessels were not chartered) onboard four vessels that ranged in length between 20 and 33 m. Up to 1,200 hooks were fished in each set on mainlines that were as long as 78 km. Three to twelve hooks were fished between floats. Buoy drops (length of line between the surface buoy and attachment to mainline) were 18–37 m long; monofilament gangions (distance from the clip on mainline to hook) were 13–64 m, most often 18–37 m in length. Sets targeting yellowfin tuna mostly used 15-0 and 16-0 circle hooks, whereas 12-0 J-hooks were used during swordfish sets. Lightsticks were used only when targeting swordfish. Soak times for each hook were determined as the elapsed time from when the baited hook went overboard to the time it was retrieved. Hook timers (Boggs, 1992) capable of recording the time a fish was caught (hook-up time) were attached to as many as 500 gangions per set. In addition, water temperature

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profiles were recorded by expendable bathythermographs (XBTs) deployed at the start and end of each set and haulback. Up to eight time–depth recorders were deployed, spaced along the length of the mainline and attached at the midpoint between buoys, to estimate the depth of each hook during the course of the soak. Instrumentation used during this experiment allowed us to determine hook-up time, hooking duration (hours hooked on the line before landing), temperature and depth of hook-up, and the thermal structure of the water column. All fish were visually assessed as dead or alive immediately after they were brought alongside the vessel. Fish were either landed or released, and their disposition (kept or discarded) was recorded. Data recorded for each hook timer included the elapsed time logged by hook timers, time of day when retrieved, and the location on the line that each fish was caught. Fish length (measured or estimated), sex (for retained catch), and detailed information on hook type and gangion length were also recorded. Logistic regression analysis (Cox and Snell, 1989) was used to predict the proportion of fish alive (by species or species group). Billfish (Istiophoridae) and sharks were analyzed as species groups because there were insufficient numbers to allow analysis of individual species. Only one dependent variable (hooking duration) was used in this analysis.

Gulf of Alaska demersal longline experiment Two commercial longline vessels (14.3 and 16.6 m in length) were chartered for this experiment in the Gulf of Alaska in 1999. Both vessels carried individual fishing quotas (IFQs) for retention of Pacific halibut (Hippoglossus stenolepis, Pleuronectidae) and sablefish (Anoplopoma fimbria, Anoplopomatidae). Limited bycatch quotas of Pacific cod (Gadus macrocephalus, Gadidae) and rockfish (Sebastes, Scorpaenidae) were permitted under the IFQs. Spiny dogfish shark (Squalus acanthias, Squalidae), various skate species (e.g., longnose skate, Raja rhina, Rajidae), and arrowtooth flounder (Atheresthes stomias, Pleuronectidae) constituted most of the bycatch and were discarded. Sixty-two longline sets were made in the Gulf of Alaska. Two hundred 12-0 circle hooks were deployed per set on 1.7 km of demersal groundline. Soak time in hours was calculated as the time elapsed between the submergence of the last hook while setting gear until the emergence of the first hook during longline retrieval. Gangions consisted of 0.5-m monofilament (136 kg test). Motion detectors (V. Afanasyev, Cambridge, UK), capable of recording up to 99 hook motions per minute, were attached to every tenth gangion during certain sets. A space of approximately 10 m on each side of these gangions was free of baited hooks to reduce the chance of recording activity from neighboring hooks. These motion detectors enabled us to determine hook-up time and hooking duration. Hook-up time was defined as the moment when more than 50 motions per minute were recorded by the detectors. This threshold level was established after viewing numerous underwater videotapes of Alaskan groundfish being captured by longline gear. Although 62 experimental longline sets were employed to evaluate the catching performance of six types (or recipes) of artificial baits against the herring bait that is often used by Alaskan longline fishers, comparisons for only one artificial bait type (#6) are presented here. Artificial baits were made of natural and biodegradable materials (Alaska Fisheries Development Foundation, 2000), and were developed exclusively for these experiments by Marco Marine (Seattle, WA) and the Center for Applied Regional Studies

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(Dr. Susan Goldhor, Cambridge, MA). These baits are not commercially available. Twelve longline sets were conducted for testing artificial bait #6; sets comprised 100 hooks baited with herring and 100 hooks baited with artificial bait #6. Bait type was alternated on every tenth hook. Groundlines included 20–30 m of free space between bait types to minimize potential interactions between different bait types on adjacent hooks.

Results Gulf of Mexico pelagic longline experiment Seventy-nine pelagic longline sets were sampled in the Gulf of Mexico between November 1994 and May 1997. Retained catch consisted of yellowfin tuna (n
485), swordfish (n
61), dolphin (Coryphaena hippurus, Coryphaenidae; n
181), wahoo (Acanthocybium solandri, Scombridae; n
47), escolar (Lepidocybium flavobrunneum, Gempylidae; n
153), bigeye tuna (Thunnus obesus, Scombridae; n
8), and bluefin tuna (Thunnus thynnus, Scombridae; n
2). There were 103 sharks recorded in the catch (Table 36.1), nearly all of which were discarded. The pelagic longlines were often soaked for long periods, in some cases, for more than 24 hours (Fig. 36.1). The proportion of fish alive when landed was inversely related to time on the line (Fig. 36.2), hence the mortality of captured fish increased as soak time increased. Of the pelagic species shown, sharks were most resistant to hooking mortality; after an initial mortality of approximately 20%, little additional mortality was observed even after 12 hours on the line. The opposite pattern was demonstrated by swordfish, most of which died on the line within 6 hours after hook-up. A number of these swordfish were shark-bitten, but it is impossible to know whether they were alive or dead when this occurred. Most swordfish in this study were discarded (70%), largely because they were below the minimum size (125 cm lower jaw–fork length). There appeared to be an initial hooking mortality of approximately 40% for yellowfin tuna on pelagic longlines. This mortality rate increased to approximately 65% after 12 hours on the line. Tuna that died on the line were either discarded or fetched a low price (due to poor quality) relative Table 36.1 Species composition of sharks caught on pelagic longlines during an experiment conducted in the Gulf of Mexico. Family

Common name

Scientific name

Carcharhinidae

Silky Oceanic whitetip Dusky Tiger Sandbar Blue Bigeye thresher Longfin mako Shortfin mako Scalloped hammerhead Unidentified

Carcharhinus falciformis Carcharhinus longimanus Carcharhinus obscurus Galeocerdo cuvier Carcharhinus plumbeus Prionace glauca Alopias superciliosus Isurus paucus Isurus oxyrinchus Sphyrna lewini Unknown

Alopiidae Lamnidae Sphyrnidae Unknown

Number 53 5 4 4 2 1 6 4 4 2 18

466

Sharks of the Open Ocean

25

Percent frequency

20

15

10

5

0 10

15

20 Mean soak time (hours)

25

30

Fig. 36.1 Frequency distribution of mean soak times for 79 pelagic longline sets in the Gulf of Mexico. Note that individual hooks may soak much longer than the mean soak time. Yellowfin Swordfish

1.0

Billfish Probability of being alive

0.8

Sharks

0.6

0.4

0.2

0.0 0

2

4

6 8 Hours after hook-up

10

12

Fig. 36.2 Results of logistic regression analysis showing the proportion of billfish (n
41), swordfish (n
46), yellowfin tuna (n
237), and sharks (n
41) alive versus length of time hooked on a pelagic longline in the Gulf of Mexico.

to individuals that were retrieved while still alive. Of the species analyzed, billfish in the family Istiophoridae (which included blue marlin, Makaira nigricans; white marlin, Tetrapturus albidus; sailfish, Istiophorous platypterus; and spearfish, Tetrapturus angustirostris) had the lowest initial hooking mortality (approximately 10%). Mortality for these species increased to 65% after 12 hours on the line.

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25

Frequency

20

15

10

5

0 0.5

1

1.5

2

2.5

3

4

5

6

7

8

9

Time elapsed before capture (hours) Fig. 36.3 Distribution of time elapsed before capture for fish caught by demersal longlines baited with herring in the Gulf of Alaska in 1999. Only results for longlines soaked for more than 6 hours are shown (range
6.5–8.9 hours; n
130 gangions). Cell ranges are: 0.5
0.5 hour; 1
0.5 to 1 hour; 1.5
1 to 1.5 hours; 2
1.5 to 2 hours; and so on.

Gulf of Alaska demersal longline experiment Two to four demersal longline sets were made on each fishing day at depths ranging from 71 to 310 m. Soak times were either short (3 hours) or long (6–9 hours). Equal numbers of short and long soaks were made on each day. Although we sampled 62 demersal longline sets that were soaked from 2.5 to 8.9 hours, only sets that were soaked in excess of 6 hours were used to examine the distribution of hook-up times for captured fish (Fig. 36.3). Furthermore, only gangions containing motion detectors and herring-baited hooks (n
130) were used to describe this distribution of hook-up times. Fish were landed on 50 of the 130 hooks associated with motion detectors (24 Pacific cod, 9 sablefish, 7 spiny dogfish shark, 4 halibut, 5 arrowtooth flounder, and 1 longnose skate); 80 hooks were hauled back with no catch. None of the landed fish were hooked beyond 3 hours after bait entered the water, even though sets included in this analysis were soaked from 6.4 to 8.9 hours. As many as 43 of the 80 empty hooks may have caught fish temporarily (i.e., for which motion detectors showed 50 motions per minute), but these escaped before longline retrieval. Figure 36.4 shows a fish that was hooked about 1 hour after the bait entered the water and that escaped 20 minutes later. Artificial bait #6 nearly eliminated the catch of sharks and skates during demersal longline fishing operations in the Gulf of Alaska, whereas the catch of target species (Pacific halibut and sablefish) using this artificial bait was similar to that using herring-baited hooks (Fig. 36.5). The difference in catch between the two baits was significant for spiny dogfish shark (paired t-test for 10 sets, p  0.005), but not significant for the target species (for 12 sets, p  0.05). Because of a limited sample size, differences were not statistically significant between bait types for catches of longnose skate (for 5 sets, p  0.05).

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100

Motions per minute

Hooked 75

50 Set

Haulback

25 Escaped 0 0:00

1:00

2:00 3:00 4:00 5:00 Time elapsed (hours:minutes)

6:00

Fig. 36.4 Movements of a single motion detector attached to a gangion on a demersal longline in the Gulf of Alaska in 1999. A fish was caught about 1 hour after the set was made and escaped 20 minutes later. This longline was retrieved about 5 hours after the fish escaped. 200 Artificial Herring

Catch (numbers)

150

100

50

0 Pacific halibut

Sablefish

Spiny dogfish shark

Longnose skate

Fig. 36.5 Demersal longline catch (number of fish by species) using herring and artificial bait #6 in the Gulf of Alaska in 1999. Comparisons were paired. Even though 12 sets were made, only sets that caught the species of interest were included for statistical analyses. Sample sizes were: Pacific halibut, n
12; sablefish, n
12; spiny dogfish shark, n
10 (two sets caught none); and longnose skate, n
5 (seven sets caught none).

Discussion Data presented in this chapter and by Boggs (1992) demonstrate that the longer fish are hooked on pelagic longlines, the more likely they will be dead upon longline retrieval. We found that hooking mortality rates were species dependent. For example, mortality of hooked fish was slow and constant for sharks but rapid for swordfish. Boggs (1992) also

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showed that the rate of hooking mortality varied among species, ranging from more than 60% mortality within 3 hours of hooking for spearfish to less than 20% mortality after 7–9 hours on the line for bigeye tuna. Overall, hooking mortality is high (greater than 80%) for species such as wahoo (Boggs, 1992), skipjack tuna (Katsuwonus pelamis, Scombridae; Boggs, 1992; Ward et al., 2004), and swordfish, whereas it is substantially lower (0–40%) for other species such as pelagic sharks (Boggs, 1992; Ward et al., 2004). Pelagic sharks, however, are sensitive to exploitation (Schindler et al., 2002); hence, even low levels of unaccounted mortality (i.e., discard mortality) could impact certain shark populations. Pelagic longlines are often soaked for 20 hours or longer during normal commercial fishing operations (Ward et al., 2004). Our results suggest that a reduction in soak time would increase the survival of discarded bycatch. However, there may be concern from the commercial fishing industry that shortened soaks may also lead to lower catches of target species. Indeed, Ward et al. (2004) showed a tendency for higher catch rates (number of fish per 1,000 hooks) as soak times increased to 20 hours. Yet their results were species dependent, and in many cases the soak time either showed no relationship to catch rate or was negatively correlated to catch rate. For example, soak time was positively correlated with catch for most shark and billfish species, whereas there was no clear relationship between soak time and catch for tuna and various bony fishes. Ward et al. (2004) showed that there was some amount of loss rate during pelagic longline fishing operations (e.g., due to escapement and bait loss) and, for many species, an optimal soaking time (less than 20 hours) that would maximize catch. We have described a study conducted in the Gulf of Alaska that utilized special instrumentation to estimate optimal soaking times for demersal longlines. This method showed that herring-baited hooks attracted fish only during the initial 3 hours of longline sets that were soaked for 6–9 hours. High (1980) and Sigler (2000) also showed a clear inverse relation between catch rate and bait soaking time for demersal longlines targeting Pacific halibut and sablefish in Alaskan waters. Sigler (2000) suggested that the reduced encounter rate over time was related to the diminishing odor concentration at the edge of the odor plume, whereas High (1980), using direct observations, showed that decreasing hook-up rate over time was caused by bait loss (e.g., bait taken by predators and scavengers such as fish, shrimp, and crab) and escapement. This rapid decline in fishing efficiency has been documented for other demersal longline fisheries. Grimes et al. (1982) observed 70% bait loss for hooks soaked for 190 minutes on the ocean bottom in the Mid-Atlantic Bight. They attributed much of this bait loss to predation by starfish (Astropectin spp.) and crabs (Cancer spp.). Our Alaska data reveal that significant numbers of targeted catch escaped, or were eaten by sharks and subsequently unmarketable. Escapement of hooked fish represents an additional reason for decreased catch over time on longlines. Data from motion detectors attached to gangions suggested that 43 of 80 empty hooks may have temporarily caught fish that managed to escape. As fish were landed on 50 hooks, this result suggests a 46% escape rate for fish striking hooks on demersal longlines. High (1980) also found significant escapement (25%) for fish that were temporarily caught on demersal longlines in Alaska. Since the incidence of escapement and the number of shark-bitten fish likely increase with the time spent hooked on longlines, and because there exists an inverse relationship between soak time and catch rates for many species (demersal and pelagic), it may not be cost-effective to fish longline gear for extended soaking periods (e.g., more than 5 hours for demersal longlines in Alaska). In pelagic longline fisheries, dead tuna are often discarded or

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fetch a lower price because of their poor quality. Since catch rates of target species decline as baits are lost, and hooked fish die or are attacked by sharks, limiting soak time to some optimal duration may be one simple way to reduce bycatch mortality while minimizing the impact to fishers’ income. Clearly, the optimal soak time will vary among fisheries. The surest method for minimizing bycatch mortality is to eliminate bycatch in the first place. Bait type is one of the most important gear parameters for species selectivity in longline fisheries (Løkkeborg and Bjordal, 1992). We showed that an artificial bait fished as well as (or better than) natural baits for target species, while the same artificial bait nearly eliminated the catch of bycatch species (e.g., sharks and rays). Others have shown speciesselective responses to bait for various demersal fisheries (Løkkeborg and Bjordal, 1992). Januma et al. (1999) developed an artificial bait for tuna longline fisheries; however, the hooking rates were lower than that of natural baits, and therefore the bait was not considered successful. Hence, virtually no successful work has been conducted in the area of speciesselective artificial baits for pelagic longline fisheries. Much more experimentation is needed to produce species-selective longline baits and longline gear. We have presented two possible approaches to reducing bycatch mortality in pelagic longline fisheries: species-selective baits and reduced soak times. However, we believe that the most effective way to reduce bycatch in a fishery is to provide fishers with incentives to develop their own solutions and to utilize useful solutions that are already available. The scientific community should assist and collaborate with the industry in developing these solutions.

Acknowledgments The Alaskan field trials were conducted in collaboration with Marco Marine (Seattle, WA), Susan Goldhor of the Center for Applied Regional Studies (Cambridge, MA), the Alaska Fisheries Development Foundation (Anchorage), and the Alaska Sea Life Center (Seward). An underwater camera system was provided by Gary Stauffer and Craig Rose of NOAA Fisheries, Alaska Fishery Science Center (Seattle, WA). We thank the captains and crews of the F/V’s Sebrika and Rocinante. This project was successful because of the work and suggestions of numerous individuals, including Chris Mitchell, Richard Drake, Susan Goldhor, Radu Giurca, Hal Cook, Mimi Fielding, Susan Inglis, Bill Coffer, Chris Moruhn, Chuck Hart, Karl Skrifvars, and Harold Kalve. The Alaska study was funded by the Alaska Science and Technology Foundation. The study conducted in the Gulf of Mexico was funded by NOAA (Salstonstall–Kennedy) Grant No. NA57FD0031 and NOAA (MARFIN) Grant No. NA47FF0019. We thank Randy E. Edwards for his collaboration in that research. We also thank the anonymous reviewers for their useful comments.

References Alaska Fisheries Development Foundation (2000) The Development of Fabricated Bait from Processed Alaskan Seafood Wastes. AFDF, Anchorage, AK, 47 pp. Boggs, C. H. (1992) Depth, capture time, and hooked longevity of longline-caught pelagic fish: Timing bites of fish with chips. Fishery Bulletin 90(4), 642–658.

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Cailliet, G. M., Holts, D. B. and Bedford, D. (1991) A review of the commercial fisheries for sharks on the West Coast of the United States. In: Shark Conservation: Proceedings of an International Workshop on the Conservation of Elasmobranchs, Taronga Zoo, Sydney, Australia, 24 February 1991 (eds. J. G. Pepperell, J. West and P. M. N. Woon). Sydney, New South Wales, Australia, pp. 13–29. Camhi, M. (1999) Sharks on the Line II: An Analysis of Pacific State Shark Fisheries. Living Oceans Program, National Audubon Society, Islip, NY, 115 pp. Cortés, E. (1999) Catch Rates of Pelagic Sharks from the Northwestern Atlantic, Gulf of Mexico, and Caribbean. ICCAT Working Document SCRS/99. Southeast Fisheries Science Center, Sustainable Fisheries Division, NMFS, Panama City, FL, 4 pp. Cox, D. R. and Snell, E. J. (1989) The Analysis of Binary Data, 2nd edn. Chapman & Hall, London, UK. Cramer, J. (1999) Large Pelagic Logbook Catch Rates for Sharks. ICCAT Working Document SCRS/99. Southeast Fisheries Science Center, NMFS, Miami, FL, 6 pp. Gillis, D. M., Peterman, R. M. and Pikitch, E. K. (1995) Implications of trip regulations for highgrading: A model of the behavior of fishermen. Canadian Journal of Fisheries and Aquatic Sciences 52, 401–415. Grimes, C. B., Able, K. W. and Turner, S. C. (1982) Direct observations from a submersible vessel of commercial longlines for tilefish. Transactions of the American Fisheries Society 111, 94–98. High, W. L. (1980) Bait loss from halibut longline gear observed from a submersible. Marine Fisheries Review 42(2), 26–29. Holts, D. B., Julian, A., Sosa-Nishizaki, O. and Bartoo, N. (1998) Pelagic shark fisheries along the West Coast of the United States and Baja California, Mexico. Fisheries Research 29, 115–125. Januma, S., Kajiwara, Y., Miura, T., Yamamoto, J. and Haruyama, M. (1999) Trial use of artificial bait with tuna longline. Bulletin of the Faculty of Fisheries, Hokkaido University 50(2), 71–76. Joyce, W. N. (1999) Management of shark fisheries in Atlantic Canada. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 74–108. Løkkeborg, S. and Bjordal, Å. (1992) Species and size selectivity in longline fishing: A review. Fisheries Research 13, 311–322. Matsunaga, H. and Nakano, H. (1999) Species composition and CPUE of pelagic sharks caught by Japanese longline research and training vessels in the Pacific Ocean. Fisheries Science 65(1), 16–22. Pawson, M. and Vince, M. (1999) Management of shark fisheries in the Northeast Atlantic. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper No. 378/1. FAO, Rome, Italy, pp. 1–46. Pikitch, E. K., Erickson, D. L. and Wallace, J. R. (1988) An Evaluation of the Effectiveness of Trip Limits As a Management Tool. Report No. 88-27. Northwest and Alaska Fisheries Center, NMFS, Seattle, WA, 33 pp. Schindler, D. E., Essington, T. E., Kitchell, J. F., Boggs, C. and Hilborn, R. (2002) Sharks and tunas: Fisheries impacts on predators with contrasting life histories. Ecological Applications 12(3), 735–748. Sigler, M. F. (2000) Abundance estimation and capture of sablefish (Anoplopoma fimbria) by longline gear. Canadian Journal of Fisheries and Aquatic Sciences 57(6), 1270–1283. Ward, P., Myers, R. A. and Blanchard, W. (2004) Fish lost at sea: The effect of soak time on pelagic longlines. Fishery Bulletin 102, 179–195.

Chapter 37

Data Collection, Research, and Assessment Efforts for Pelagic Sharks by the International Commission for the Conservation of Atlantic Tunas Elizabeth A. Babcock and Hideki Nakano

Abstract The International Commission for the Conservation of Atlantic Tunas (ICCAT), a regional fishery management organization, is the primary repository of fisheries data for tuna-like species in the Atlantic Ocean. Since the mid-1990s, ICCAT has been collecting shark fishery statistics, including catch and effort data, as well as information from tagging and biological studies of pelagic sharks. The catch data, particularly before the 1990s, are incomplete, and often do not separate sharks by species. Nevertheless, in 2004, the ICCAT bycatch subcommittee conducted an assessment of the status of blue sharks (Prionace glauca) and shortfin mako sharks (Isurus oxyrinchus) in the Atlantic. The assessment indicated that blue sharks appear to be well above the biomass that would sustain maximum sustainable yield (BMSY) in both the North and South Atlantic. Shortfin mako sharks have declined in both regions, and may be below BMSY in the North Atlantic. Because of the limitations in the catch data, the subcommittee considered the assessment to be provisional. Key words: ICCAT, data collection, assessment, international treaties, management.

Introduction The International Commission for the Conservation of Atlantic Tunas (ICCAT) was established in 1969, based on an international convention, for the purpose of conserving “tuna and tuna-like fishes” (i.e., tunas and swordfish) in the Atlantic (ICCAT, 2003). Because sharks are caught incidentally by tuna and swordfish fisheries, ICCAT also became a repository for information on sharks. ICCAT began to play a more formal role in collecting shark data in 1995, after the Convention on International Trade in Endangered Species of Flora and Fauna (CITES) passed CITES Resolution 9.17, which requested the assistance of the Food and Agriculture Organization (FAO) of the United Nations, ICCAT, and other Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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regional fisheries management organizations in compiling information on the “biological and trade status of sharks subject to international trade.” In response, that same year ICCAT passed Resolution 95-2 entitled “Resolution by ICCAT on Cooperation with the Food and Agriculture Organization of the United Nations with Regard to Study on the Status of Stocks and By-catches of Shark Species.” This resolution called on the contracting parties of ICCAT to provide FAO with the information required to “initiate a program to collect, on a global scale, the necessary biological data, including stock abundance and the magnitude of bycatch, and trade data on shark species.” In 1995, ICCAT also formed a subcommittee on bycatch, with a mandate to incorporate bycatch information into the ICCAT database (Miyake, 2001). This subcommittee developed a reporting format for bycatch data, and requested that the member nations report bycatch annually (ICCAT, 1997; Miyake, 2001). Since then, the subcommittee has identified the species caught as bycatch in tuna fisheries (ICCAT, 2000; Table 37.1), developed a database of shark catches (ICCAT, 2004), convened a meeting to determine whether data were sufficient to assess the status of any pelagic shark species (ICCAT, 2002), and conducted preliminary assessments of blue (Prionace glauca, Carcharhinidae) and shortfin mako (Isurus oxyrinchus, Lamnidae) sharks in June 2004 (ICCAT, 2005). Because ICCAT had already asked its members to submit total catch (TASK I) and catch and effort by area and period (TASK II) fishery statistics for tuna and billfishes, the group decided that similar data should be requested for sharks. The ICCAT database now includes total catches (including discards), by fleet, species, and statistical area, catches by 5⫻5-degree areas and quarter of the year for some fleets, effort and catch per unit effort (CPUE) for some fleets, morphometric measurements such as length–weight relationships, and tag-and-release data (Miyake, 2001). Not all fleets reporting tuna and swordfish catches have been reporting shark catches. For example, between 2000 and 2003, of the 81 flags in the ICCAT TASK I database, 34 of them, representing 25% of the finfish catches, reported no shark catches (ICCAT, 2004). In addition, some fleets that have been reporting shark catches since the mid-1990s have been Table 37.1 Pelagic shark and ray species reported to ICCAT, by fishing gear (ICCAT, 2000).* Scientific name

Common name

Longline

Gill net

Purse seine

Harpoon Trap Other

Pteroplatytrygon violacea Alopias superciliosus Alopias vulpinus Carcharhinus falciformis Carcharhinus longimanus Isistius brasiliensis Isurus oxyrinchus Isurus paucus Lamna nasus Prionace glauca Pseudocarcharias kamoharai Zameus squamulosus

Pelagic stingray Bigeye thresher Common thresher Silky Oceanic whitetip Cookiecutter Shortfin mako Longfin mako Porbeagle Blue

X X X X X

X X X X

X

X X X

X X X X

X X X X

Crocodile Velvet dogfish

X X

*

X X X X

X

X

X X

X

X

X

X X X

Baitboats reported no catches of pelagic sharks. An additional 11 skates and rays and 42 coastal sharks were also reported, including white shark (Carcharodon carcharias, Carcharhinidae), which was caught with every gear except baitboat.

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unable to estimate their historical shark catches before 1995. In comparing the ICCAT and FAO data on sharks, Miyake (2001) noted that the ICCAT data include discards (which are not reported to FAO) and have a greater part of the catch identified to species. In 2001, the subcommittee concluded that, although there were gaps in the historical data, there would be sufficient information in 2004 to assess both blue and shortfin mako sharks (ICCAT, 2002). These two species were chosen because they are commonly caught (Fig. 37.1), had not been previously assessed, and were widely distributed, so there was little chance that coastal nations could assess them without the involvement of international fishery management organizations (ICCAT, 2002). Although longfin mako sharks (Isurus paucus, Lamnidae) are sometimes caught by the tuna longline fishery, the group judged this catch to be negligible. Porbeagles (Lamna nasus, Lamnidae), which are not as widely distributed, had already been assessed in the Northwest Atlantic by scientists from Canada (ICCAT, 2002; Campana et al., 2008). Following this meeting, ICCAT passed Resolution 01-11 entitled “Resolution by ICCAT on Atlantic Sharks,” which requested contracting parties and others to (1) submit catch and effort data for porbeagle, shortfin mako, and blue sharks, (2) encourage the live release of incidentally caught sharks, (3) minimize waste and discards of sharks, and (4) “voluntarily agree not to increase fishing effort targeting Atlantic porbeagle, shortfin makos and blue sharks until sustainable levels of harvest can be determined through stock assessments.”

Assessment of blue and shortfin mako sharks When the ICCAT bycatch subcommittee met again in 2004 to produce an assessment of blue and shortfin mako sharks in the Atlantic, the catch data were improved but still incomplete (ICCAT, 2005). Every tuna or swordfish fishery would be expected to catch at least some pelagic sharks, but many nations have submitted no shark catch data, or have submitted catch data only for recent years. For example, Spain reported no catches of blue sharks until

Carcharhinus falciformis Alopias spp.

Carcharhinus longimanus Isurus spp. Lamna nasus

Prionace glauca

Coastal and unidentified sharks Pelagic sharks Fig. 37.1 Shark catches reported to ICCAT by species or category, from 1995 through 1999 (ICCAT, 2004).

Catch (t)

Data Collection, Research, and Assessment by ICCAT

80,000

Reported

70,000

High estimated

60,000

Low estimated

475

50,000 40,000 30,000 20,000 10,000 0 1971

12,000

Catch (t)

10,000

1976

1981

1986 Year (a)

1991

1996

2001

Reported Estimated

8,000 6,000 4,000 2,000 0 1971

1976

1981

1986 Year

1991

1996

2001

(b) Fig. 37.2 Catch estimates for the North and South Atlantic combined for (a) blue sharks and (b) shortfin mako sharks (ICCAT, 2005).

1997, and catches of 20,000–30,000 metric tons per year from 1997 to 2002, accounting for 80% of the total catch of blue sharks over the entire database (ICCAT, 2005). Without estimates of the complete historical catches, it is impossible to produce a realistic assessment of the trend in population status using any method that depends on accurate catch data. The group discussed several ways to estimate missing shark catches, for example, by using catch rates from observer data, or from nations with more complete data. In the end, the subcommittee produced estimates of unreported shark catches by assuming that the ratio of shark catches to tuna and swordfish catches would be the same as the average ratio in recent years for fleets reporting shark catches, which is 4.28:1. This ratio was also adjusted for changes in targeting based on the ratios of tuna and swordfish in the catch (ICCAT, 2005; Fig. 37.2). The subcommittee produced separate preliminary assessments of the status of North and South Atlantic stocks of both species. The Mediterranean was considered a separate stock and was not assessed because of lack of data. Those stock units were assumed by the group based on distribution and tag-and-recapture information. The available indices of abundance were CPUE series from the longline fisheries of Japan, Taiwan, the United States, and Brazil. Many local indices were also presented at the meeting from US recreational

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Sharks of the Open Ocean

fisheries, and from fisheries in Canada, Ivory Coast, and Ireland. The indices that were more wide-ranging and represented large catches were used in the assessment models (shortfin mako, North: Japanese longline, US longline; shortfin mako, South: Japanese longline, Brazil Southeast longline; blue shark, North: Japanese longline, US longline; blue shark, South: Japanese longline, Chinese Taipei longline, Brazil Southeast and Northeast longline; ICCAT, 2005). Demographic data were available for both species, although there was debate about the length of the reproductive period for each. The group produced updated estimates of the intrinsic rate of population increase (r) and other parameters based on the Monte Carlo simulation of Leslie matrix models (Cortés, 2008). The demographic information was used to develop inputs for the assessment models, such as prior probability distributions for r and adult natural mortality rate M. Three assessment models were applied: (1) a Bayesian surplus production (BSP) model fitted to CPUE data and requiring catch data, (2) an age-structured model fitted to CPUE data and requiring catch data, and (3) a “catch-free” age-structured model fitted to CPUE data. The age-structured model was applied only to North Atlantic blue sharks because of insufficient data for other stock units. The BSP model was applied to all four stocks, and the catch-free model was applied to all stocks except shortfin mako sharks in the South Atlantic. For blue sharks, the CPUE indices were quite variable and showed no particular trend in the North or South Atlantic. Thus, the BSP, age-structured, and catch-free models all estimated that the current population was above the biomass that would produce maximum sustainable yield (BMSY). Because of the many assumptions that went into the CPUE indices and (for the BSP and age-structured models) the catch estimates, these results are considered highly uncertain and only preliminary in nature. For shortfin mako sharks, the abundance indices showed a decline in both the North and South Atlantic. The BSP model estimated that the population remained above BMSY. The catch-free model, on the other hand, estimated that shortfin mako in the North Atlantic had declined more than 50% since 1970, implying that the population may be overfished (ICCAT, 2005).

Conclusions The 2004 ICCAT assessment indicated that there may be some cause for concern for shortfin mako sharks, but probably not for blue sharks. These results depend on the assumptions that were made in the models and data, particularly in estimating the historical catches. The bycatch subcommittee recommended that ICCAT member nations continue to improve the catch data series and other information needed to assess the status of pelagic sharks. Following this assessment, ICCAT passed Resolution 04-10, which effectively bans the practice of finning sharks (i.e., retaining the fins and discarding the rest of the shark) by requesting member nations to require full utilization of sharks, require vessels to not have fins that total more than 5% of the weight of sharks onboard, and require live release of incidentally caught sharks. The resolution also calls for additional shark research and data collection. ICCAT’s efforts since 1995 have improved our understanding of the biology and status of pelagic sharks in the Atlantic, including distribution, species composition, segregation

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by sex and size, and the impacts of fisheries on their populations, and have identified gaps in the available data. Continuing efforts are needed to fill in the historical catch series from all member countries and particularly those with large fleets, resolve the uncertainties regarding stock structure and demographics, and derive unbiased indices of abundance. Independent sources of information, such as tagging databases (ICCAT, 2005), fishery-independent surveys (e.g., Simpfendorfer et al., 2002; Baum and Myers, 2004), and trade data (e.g., Clarke, 2004), could provide such unbiased indices. The next ICCAT assessment of blue and mako sharks is expected to take place in 2008.

References Baum, J. and Myers, R. A. (2004) Shifting baselines and the decline of pelagic sharks in the Gulf of Mexico. Ecology Letters 7, 135–145. Campana, S. E., Joyce, W., Marks, L., Hurley, P., Natanson, L. J., Kohler, N. E., Jensen, C. F., Mello, J. J., Pratt Jr., H. L., Myklevoll, S. and Harley, S. (2008) The rise and fall (again) of the porbeagle shark population in the Northwest Atlantic. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Clarke, S. (2004) Understanding the pressures on fishery resources through trade statistics: A pilot study of four products in the Chinese dried seafood market. Fish and Fisheries 5, 53–74. Cortés, E. (2008) Comparative life history and demography of pelagic sharks. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. ICCAT (1997) Report of the First Meeting of the Shark Working Group of the ICCAT Sub-committee on By-catch, Miami, FL, 26–28 February 1996. ICCAT Collective Volume of Scientific Papers 46(4), 289–371. ICCAT (2000) Report of the Inter-sessional Meeting of the ICCAT Sub-committee on By-catch, Messina, Italy, 11–14 May 1999. ICCAT Collective Volume of Scientific Papers 51(1), 1728–1775. ICCAT (2002) ICCAT Data Preparatory Meeting for Atlantic Shark Stock Assessment, Halifax, Nova Scotia, Canada, 11–14 September 2001. ICCAT Collective Volume of Scientific Papers 54(4), 1064–1106. ICCAT (2003) International Commission for the Conservation of Atlantic Tunas. Basic texts, 3rd revision. www.iccat.es, accessed 23 September 2005. ICCAT (2004) Shark database, and TASK I catch database. www.iccat.es, accessed 23 September 2005. ICCAT (2005) Report of the 2004 Inter-sessional Meeting of the ICCAT Sub-committee on By-catches: Shark Stock Assessment, Tokyo, Japan, 14–18 June 2004. ICCAT Collective Volume of Scientific Papers 58(3), 799–890. Miyake, P. M. (2001) ICCAT effort on research on shark incidental-catches of tuna fishing fleets. ICCAT Collective Volume of Scientific Papers 52(1), 1553–1557. Simpfendorfer, C. A., Heuter, R. E., Bergman, U. and Connett, S. M. H. (2002) Results of a fisheryindependent survey for pelagic sharks in the western North Atlantic, 1977–1994. Fisheries Research 55, 175–192.

Chapter 38

Pelagic Sharks and the FAO International Plan of Action for the Conservation and Management of Sharks Rachel D. Cavanagh, Sarah L. Fowler and Merry D. Camhi

Abstract In 1999, the United Nations Food and Agriculture Organization (FAO) Committee of Fisheries adopted the International Plan of Action for the Conservation and Management of Sharks (IPOA-Sharks). Since 2001, the IUCN Shark Specialist Group, with assistance from TRAFFIC, has been monitoring its implementation and reporting back to the Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES). Most countries have made little or no progress with implementation. To date, of 113 States reporting elasmobranch landings to FAO, only 8 have adopted their National Plan of Action for Sharks, and at least 16 more have theirs drafted. The few available national and regional Shark Plans vary widely in quality, with many failing to meet some of the recommended standards. This chapter describes the debates and policies that resulted in the adoption of the IPOA-Sharks, reviews progress since 1999, and highlights its relevance in improving the management status of pelagic sharks. Key words: IPOA, NPOA, Shark Plan, SAR, CITES, COFI, conservation, management.

Introduction Chondrichthyan fishes include sharks and their relatives – skates, rays, and chimaeras, all referred to in this chapter as “sharks.” (The term “elasmobranchs” – i.e., sharks, skates, and rays – is sometimes used in this chapter when referring to the United Nations Food and Agriculture Organization (FAO) data.) They generally have limited capacity to recover from intense exploitation because of their conservative life histories, which are characterized by slow growth, late age at maturity, low fecundity, and low natural mortality (Musick, 1999). Sharks have received less research, conservation, and fisheries management attention than the many commercially fished teleost fishes because of their historically low economic value, relatively low world production, and general negative image (Walker, 1998). Conservation efforts have been seriously hampered by a lack of knowledge Sharks of the Open Ocean: Biology, Fisheries and Conservation. Edited by M. D. Camhi, E. K. Pikitch and E. A. Babcock © 2008 Blackwell Publishing Ltd. ISBN: 978-0632-05995-9

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of shark biology and inadequate shark fishery data (Pawson and Fowler, 2001). Most States have no requirement to record shark catches or to provide a species breakdown of the catch from their fisheries, including most pelagic fisheries (FAO, 2000). Species such as blue (Prionace glauca, Carcharhinidae), shortfin mako (Isurus oxyrinchus, Lamnidae), and oceanic whitetip (Carcharhinus longimanus, Carcharhinidae) sharks are known to range across entire ocean basins (Stevens and Wayte, 1999; Boustany et al., 2008; Kohler and Turner, 2008), further complicating research, management, and monitoring (Baum and Myers, 2008). Although there is an overall lack of information on population status, enough is certainly known to warrant immediate management attention for pelagic shark stocks (Camhi, 2008). Pelagic sharks are caught predominantly as bycatch in longline, purse-seine, and driftnet fisheries targeting tuna and billfishes on the high seas and in States’ exclusive economic zones (EEZs; usually out to 200 nautical miles from shore). Historically, much of the lowervalued shark catch was discarded, usually without record (Walker, 1998). The growing demand for highly valuable shark fins and other products has led to dramatic increases in the targeting of sharks. Indeed, purported bycatch fisheries often capitalize on the lack of shark fishery management and in some cases may modify their gear to target sharks, leading to levels of exploitation similar to those in directed fisheries (Clarke, 2003; Aires-da-Silva et al., 2008). There has been a proliferation in the practice of finning (removal of a shark’s fins and discarding of the carcass at sea) in many fisheries. This occurs because shark fins have high value, take up little hold space, and are easy to process and store, while their carcasses are generally of low market value and may taint the flesh of the far more valuable tuna and billfish that are stored in the same hold. Approximately one-third of the identifiable fins moving through Hong Kong fin markets are believed to be from pelagic shark species (Clarke, 2003; Clarke et al., 2006). Despite the increasing awareness and concern that have led to important international shark conservation and management initiatives in recent years, at present there are few effective international management mechanisms in place for sharks (Fowler and Cavanagh, 2005; Camhi et al., 2008a). This chapter describes the debates and policies that resulted in the adoption of the FAO International Plan of Action for the Conservation and Management of Sharks (IPOA-Sharks), and it discusses progress with the IPOA-Sharks and its relevance to improving the management status of pelagic sharks. The Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES) established the legal framework for the prevention of trade in endangered species and for effective regulation of international trade in other listed species that may become threatened in the absence of such regulation. Resolution Conference 9.17, Status of International Trade in Shark Species, was adopted at the Ninth Conference of the Parties (CoP9) to CITES in 1994, in response to widespread concern about expanding, unmanaged fisheries for sharks, the impact of rising volumes of shark fins entering international trade, the vulnerability of sharks to fishing pressure, and evidence of declining stocks. Through this Resolution, CITES requested a review on the status of sharks and the effects of international trade, and requested that FAO and other international fisheries organizations improve their research programs. Further progress was made at CoP10 (1997) with Decision 10.93 (directed to FAO), Decision 10.74 (directed to the Chairman of the CITES Animals Committee), and Decision 10.126 (directed to the CITES Secretariat)

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regarding the development and proposal of guidelines leading to the IPOA for the conservation and effective management of sharks (www.cites.org; Fowler and Cavanagh, 2005). (The CITES Plants and Animals Committees generally meet once a year to provide technical support and expert information regarding species subject to, or that may become subject to, CITES controls. The Committees formulate advice, make recommendations, and draft resolutions.) In response to the CITES action on sharks, the FAO Committee on Fisheries (COFI; the only global intergovernmental forum examining major international fisheries and aquaculture issues) acknowledged that it was necessary to control directed shark fisheries and fisheries in which sharks constitute a significant bycatch, consistent with the FAO Code of Conduct for Responsible Fisheries, agreements from the 1995 United Nations Conference on Straddling Fish Stocks and Highly Migratory Fish Stocks, and any applicable rules of international law (Fowler and Cavanagh, 2005). In 1999, COFI adopted the IPOA-Sharks. This agreement, which is wholly voluntary, encompasses all chondrichthyan fisheries and applies to States wherever their fleets are catching sharks, directed or as bycatch, within EEZs or on the high seas. The overall objective is to ensure the conservation and management of sharks and their long-term sustainable use through improved species-specific data collection on catches, landings, and trade, and the monitoring and management of their fisheries. The IPOA-Sharks called upon individual States and those participating in bilateral and multilateral agreements, as well as the relevant regional fisheries organizations (RFOs), to carry out regular assessments of the status of their shark stocks through a Shark Assessment Report (SAR; Table 38.1). The IPOA further requested those States whose fisheries take sharks to develop and implement a National Plan of Action for Sharks (NPOA, or “Shark Plan”) by the COFI session in 2001 (Table 38.2). The IPOA encouraged coordinated, joint Plans of Action among States with subregional arrangements or members of RFOs. Such coordination is particularly important for pelagic sharks, whose transboundary, highly migratory, and high-seas stocks are often exploited by more than one State. Once implemented, States and RFOs are encouraged to evaluate the effectiveness of their Shark Plans every 4 years, and to make cost-effective adjustments to improve them where necessary. Detailed technical guidelines to support development and implementation of the IPOASharks are available and provide guidance on monitoring, data collection and analysis, research, building capacity, and implementation of management measures (FAO, 2000). Table 38.1 Suggested contents for a Shark Assessment Report in fulfillment of the FAO IPOA-Sharks (FAO, 2000). SAR content Past and present trends in: – Fishing effort in both directed and nondirected fisheries – Yield: physical and economic Status of stocks Existing management measures: – Control of access to fishing grounds – Technical measures (e.g., bycatch reduction measures, existence of sanctuaries, and closed seasons) – Monitoring, control, and surveillance Effectiveness of management measures Possible modifications of management measures

• • • • •

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Table 38.2 The aims and suggested content of a National Plan of Action (NPOA) (FAO, 2000). Shark Plan aims Ensure that shark catches from directed and nondirected fisheries are sustainable Assess threats to shark populations, determine and protect critical habitats, and implement harvesting strategies consistent with the principles of biological sustainability and rational long-term economic use Identify and provide special attention, in particular to vulnerable or threatened shark stocks Improve and develop frameworks for establishing and coordinating effective consultation involving all stakeholders in research, management, and educational initiatives within and between States Minimize unutilized incidental catches of sharks Contribute to the protection of biodiversity and ecosystem structure and function Minimize waste and discards from shark catches (e.g., by requiring the retention of sharks from which fins are removed) Encourage full use of dead sharks Facilitate improved species-specific catch and landings data and monitoring of shark catches Facilitate the identification and reporting of species-specific biological and trade data

• • • • • • • • • • Shark Plan content of prevailing state of: • Description – Shark stocks and populations • •

– Associated fisheries – Management framework and its enforcement Objective of the NPOA Strategies for achieving objectives

Progress Progress toward implementation of the IPOA-Sharks by shark-fishing States and RFOs has been disappointingly slow, with only 24 States (plus the European Union) reporting either completion of a draft or adoption of their national Shark Plan at the time of writing (Table 38.3). NPOAs are usually drafted or commissioned by a State’s fisheries agency, then must be approved and officially adopted by the State, after which implementation can begin. This often slow but dynamic process can prove difficult to track because relevant documents and steps are not always made public. Readers are referred to the IUCN Shark Specialist Group (SSG) and FAO Web sites for future updates (see www.flmnh.ufl.edu/ fish/organizations/ssg/ssg.htm and www.fao.org/figis/servlet/static?dom⫽org&xml⫽ipoa_ sharks.xml). The following provides a brief review of steps taken toward IPOA implementation since 2001. 2001: At the COFI meeting in February 2001 (the deadline set by FAO for States to develop and implement NPOAs), only 29 of the 113 States that provide shark catch data to FAO had reported any progress with IPOA implementation. Of these, just 6 had an SAR or NPOA available for review: Australia (draft SAR), the European Union (draft NPOA), Italy (draft NPOA), Japan (NPOA), Seychelles (FAO-commissioned case study; Nageon de Lestang, 1999), and the United States (NPOA). Each of these NPOAs failed to meet some of the standards recommended by FAO. 2002: By September 2002, little progress had been made by States and only a few RFOs had implemented specific measures for sharks (IUCN/SSC SSG and TRAFFIC, 2002a, b). In response to concerns raised at CITES CoP12 in November 2002, FAO acknowledged the negligible progress (Cochrane, 2003). CITES Parties then adopted

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Table 38.3 Progress toward implementation of FAO’s IPOA-Sharks for all major shark-fishing States (defined as ⬎10,000 t of elasmobranch landings in 2002, shown in italics) and others known to have adopted, drafted, or begun drafting their NPOAs as of May 2007. Country

NPOA adopted a,c

Argentina Australiab Brazil c Brunei Darussalamd Cambodiad Canada f Cape Verdee Chilec Colombiac Ecuador c,f European Uniong Franceg Guineae Guinea-Bissaue Indiaa Indonesiad Italyg Japand,f Malaysiad,f Maldives Mauritaniae Mexicof Myanmard Namibia New Zealand a,f Nigeriaa

冑

冑

冑

冑

冑 冑

Pakistana Perua,c Philippinesd Portugalg Republic of Koreaa Senegale Seychellesf Sierra Leonee South Africaa Spaing Sri Lankaa Taiwanh Thailandd The Gambiae United Kingdomf,g

冑

Status of NPOA Reported working toward NPOA NPOA adopted, May 2004 NPOA drafted, 2006; awaiting adoption Reported working on drafting NPOA, October 2005; current status unknown NPOA process began in 2005 but has stalled NPOA adopted, March 2007 NPOA drafted, 2006 NPOA drafted and awaiting government approval Initiated work on NPOA in 2006 NPOA adopted, May 2005 Preliminary draft in 2001, Community Shark Plan in preparation Will be covered by EU Community Plan in preparation NPOA drafted, 2006 NPOA drafted, 2006 Reported working toward NPOA; current status unknown NPOA in preparation since 2005; current status unknown NPOA drafted, 2000, but will be covered by EU Community Plan in preparation NPOA adopted, February 2001 NPOA drafted, February 2005, and projected for adoption in 2006 No information on IPOA-Sharks implementation, but some sharkfishing activities are regulated NPOA drafted, 2006 NPOA adopted, 2004; awaiting implementation Reported working on drafting NPOA, October 2005; current status unknown NPOA adopted, 2004 NPOA drafted, 2007 (public comment through February 2008) Not working toward IPOA-Sharks implementation as of 2004; current status unknown Reported working toward NPOA; current status unknown Reported working toward NPOA; current status unknown Had not begun drafting NPOA as of October 2005; current status unknown Will be covered by EU Community Plan in preparation Reported planning to develop NPOA in 2004; current status unknown NPOA drafted, 2006 NPOA drafted, 2005; implementation projected for 2007 NPOA drafted, 2006 NPOA draft should be completed in 2007 and published in 2008 Will be covered by EU Community Plan in preparation Not working toward IPOA-Sharks implementation in 2004; current status unknown NPOA adopted, May 2006 NPOA drafted, October 2005, and entering implementation in 2006 NPOA drafted, 2006 NPOA drafted, August 2004, but will be covered by EU Community Plan in preparation (Continued)

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Table 38.3 (Continued). Country i

United States Uruguayc Venezuelac Vietnamd

NPOA adopted

Status of NPOA

冑

NPOA adopted, February 2001 Initiated work on NPOA in 2006 NPOA drafted, under discussion with government authorities Reported working on drafting NPOA, October 2005; current status unknown

a

Status of NPOA for these States is reported in Anonymous (2004b). Australia’s NPOA (Shark Advisory Group and Lack, 2004) is available at www.daffa.gov.au/fisheries/ environment/bycatch/sharkplan. c Brazil’s NPOA (in Portuguese) is available at www.sbeel.org.br. For NPOA status for Latin American States, see www.sur.iucn.org/listaroja/boletin/boletin11/11articulo4.htm. d SEAFDEC has a regional initiative under way working toward IPOA implementation (SEAFDEC, 2006). All members agreed to have a draft NPOA available by January 2005, but only Japan, Malaysia and Thailand’s (Lack and Sant, 2006) were drafted as of December 2006. The Thai draft was not available at time of writing; Malaysia draft NPOA is available at www.fao.org/figis/servlet/static?xml⫽ipoa_sharks.xml& dom⫽org&xp_nav⫽3. e The West African Sub-Regional Commission on Fisheries (CSRP) initially produced a subregional Shark Plan endorsed by the sub-region’s fisheries ministers and has since encouraged Member States to develop their own NPOAs. f The NPOAs of Canada (DFO, 2007), Ecuador (Aguilar et al., 2005), Japan (Government of Japan, 2001), Malaysia (Malaysia Department of Fisheries, 2005), Mexico (CONAPESCA, 2004), New Zealand, Seychelles (Nevill et al., 2007; Lucas and Gamblin, 2006), and United Kingdom (Fowler et al., 2004) are available through the FAO Web site: www.fao.org/fi/website/FIRetrieveAction.do?dom⫽org&xml⫽ipoa_sharks.xml. g Will be included in the EU Community Plan, which will cover 27 countries. h Taiwan’s NPOA (Taiwan Fisheries Agency, 2006) is available at www.fa.gov.tw/eng/guide/npoasharke.php. i The US NPOA (NMFS, 2001) is available at www.nmfs.noaa.gov/sfa/Final%20NPOA.February.2001.htm. b

Decision 12.49: “The Secretariat shall encourage CITES authorities of Parties to obtain information on IPOA-Sharks implementation from their national fisheries departments and report on progress at future meetings of the [CITES] Animals Committee.” In addition, CITES Resolution Conference 12.6, Conservation and Management of Sharks, directed “the Chairman of the Animals Committee to monitor the implementation of the IPOASharks.” Other relevant action points are outlined in the report of the CITES Animals Committee Intersessional Working Group on Sharks (Anonymous, 2004a). 2003: Reports on IPOA progress at COFI in early 2003 revealed that monitoring and management of shark fisheries were still woefully inadequate. At the 19th Meeting in 2003, the CITES Animals Committee Shark Working Group (Anonymous, 2003a) requested that the CITES Secretariat obtain further information from Parties on any progress (Anonymous, 2003b, c) and that the IUCN SSG produce a report summarizing the results (Anonymous, 2004b). 2004: The IUCN SSG provided CITES Parties, through the Animals Committee, with detailed analyses of progress by all shark-fishing States. Although twice as many States had reported progress toward implementation of the IPOA-Sharks as in 2002, with particularly good progress by some African range States, there was little evidence of any improved shark fisheries management resulting from this activity. It was noted that, if all the provisions of Resolution Conference 12.6 are to be implemented, “it is important for

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the Animals Committee not only to monitor the delivery of Shark Plans and assessments by Parties, but to determine how many States are actually managing their shark fisheries as a result, and hence whether the implementation of the IPOA-Sharks has led to any real improvement in the conservation and management status of shark fisheries and populations in the wild” (Anonymous, 2004c). 2005: In March 2005, COFI reported that only 11% of its Member States had developed and implemented their Shark Plans (FAO, 2005). An expert consultation was held in December 2005 to identify progress toward, deficiencies in, and actions needed to improve implementation of the IPOA (FAO, 2006). Concern was raised that some fishing States may regard the drafting of an NPOA alone as fulfillment of their IPOA obligations: This may help explain why so few concrete management actions for sharks have been implemented to date. The consultation also confronted, without resolution, the limitation posed by the voluntary nature of the IPOA and suggested that the IPOA-Sharks initiative needed to be reinvigorated. To date, of 113 States reporting shark landings to FAO, 66 States plus the European Union (EU) have indicated some degree of progress toward IPOA implementation (Anonymous, 2004b); 24 States plus the EU are known to have produced a draft of their NPOA Shark Plan, an increase from 12 States in 2004 (Table 38.3). Yet only 8 of these States have gone on to adopt their NPOAs. Of the 22 major shark-fishing States (defined as reporting ⬎10,000 t in elasmobranch landings to FAO in 2002; FAO, 2004), 5 have adopted their NPOAs (Canada, Japan, Mexico, Taiwan, and the United States) and 5 have produced NPOA drafts that are awaiting adoption (Brazil, Malaysia, New Zealand, Thailand, and the United Kingdom). Of the 12 remaining major shark-fishing States in 2002, 8 (Argentina, India, Indonesia, Pakistan, and Peru, and France, Portugal, and Spain as part of the European Union) have indicated that they are working toward the implementation of the IPOA (Table 38.3). No clear progress toward the IPOA has been reported, however, for the Maldives, Nigeria, Republic of Korea, or Sri Lanka. Australia, Ecuador, and Namibia are the only States reporting fewer than 10,000 t landings per year that have already adopted their NPOAs. A number of other states, however, have finalized drafts or have drafts in progress (Table 38.3). It should be noted that the European Union has most recently been charged by the EU Parliament to produce a draft Community Action Plan for sharks by the end of June 2007 (Lack and Sant, 2006). This plan, which has been under development since 2001, will apply to all 27 Member States of the European Union, of which 4 are major shark-fishing nations: Spain, France, the United Kingdom, and Portugal. As a noteworthy example of regional cooperation, by mid-2006, 7 States of the SubRegional Commission on Fisheries (CSRP) in West Africa (Cape Verde, Guinea, GuineaBissau, Mauritania, Senegal, Sierra Leone, and The Gambia) had finalized drafts of their NPOA and are in the process of adoption. Of the 11 Member States of the Southeast Asian Fisheries Development Center (SEAFDEC), 4 are major shark-fishing nations: Japan, Indonesia, Malaysia, and Thailand. SEAFDEC produced a framework to promote IPOA-Shark implementation in their region (Japan had previously adopted its NPOA) and to guide Member States in the formulation of their NPOAs. As a result, by October 2005, Malaysia and Thailand had completed drafts of

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their NPOAs, while Brunei Darussalam, Cambodia, Indonesia, Myanmar, the Philippines, and Vietnam were in various stages of NPOA development (SEAFDEC, 2006). The available NPOAs vary greatly in scope: Some are highly comprehensive and forward thinking, while others present a brief snapshot of current shark fisheries (IUCN/ SSC SSG and TRAFFIC, 2002a, b). Similarly, it is difficult to determine from available information the degree to which adopted NPOAs are actually being implemented by their governments.

Discussion While the lack of national and regional plans developed under the IPOA-Sharks is troubling, even the most detailed of Shark Plans will not improve shark fisheries management if they are not effectively implemented and enforced. Although fisheries management practices and capacities vary widely by country, some of the difficulties impeding implementation of the IPOA-Sharks and other shark management measures are not trivial and are likely common to many shark-fishing States. These difficulties are summarized below.

Lack of political will The slow progress in IPOA-Sharks implementation appears to be rooted in both a lack of awareness about the vulnerability of shark populations to fishing pressure and a lack of political will to ensure their sustainability. The latter may arise because, with a few exceptions, shark fisheries contribute relatively little to the total fisheries landings of most States, in either volume (usually ⬍1%) or economic value. This makes national investment in sustainable shark fisheries management a much lower priority than for species that support more important and dependable fisheries, especially when financial resources and management capacity are limited. Although shark fins, particularly those from highly desirable species, are now among the most expensive seafood products and retail from US $4.25 up to $744/kg (Clarke, 2002, 2003), most of the economic benefits accrue outside the State in whose waters they were originally taken. Furthermore, the voluntary nature of the IPOA-Sharks generates little incentive to invest resources in NPOA development and implementation. In an effort to confront this problem, the UN General Assembly adopted Resolutions on Sustainable Fisheries (UN General Assembly, 2005) that call upon fishing States and fisheries management organizations to implement the IPOA-Sharks as a matter of priority and to assist other States in doing so. Slow progress for shark fisheries management between these sessions, especially by developed States and RFOs that do have the baseline data and technical resources to implement the IPOA-Sharks, underscores this lack of political will. There is, however, a ray of hope: Since 2004, a number of RFOs have adopted by consensus several binding measures aimed at stopping shark finning in fisheries under their purview (see below). Although bans on finning are an important step forward, they must be enforced to be effective, and even then should be recognized as only a first step toward more precautionary management (such as species-specific quotas) to ensure the sustainability of pelagic shark fisheries (Lack and Sant, 2006).

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Lack of technical capacity Another equally important constraint to IPOA-Sharks implementation is the lack of technical capacity to institute the monitoring and management measures envisaged by FAO, even when the political will exists. Many of the relevant government departments lack the expertise and/or have insufficient staff resources; there may also be a dearth of baseline data upon which to base management. For developing States that lack the capacity to take action, significant technical assistance from FAO and/or States with the technical expertise in shark fisheries management is essential. A lack of data or uncertainty regarding data sets, however, is no excuse for inaction, especially when FAO recognizes adaptive, data-poor management measures as appropriate under these circumstances. The IPOA-Sharks guidelines clearly state that an NPOA should include strategies for improving data collection (see Table 38.2) and can be used to initiate an incremental approach to achieving sustainable shark fisheries management. The IPOA complements the precautionary approach (embodied in the 1995 UN Agreement on Straddling and Highly Migratory Fish Stocks and the 1995 FAO Code of Conduct for Responsible Fisheries), which requires that caution be applied when data are insufficient or unreliable, and calls on fishery managers to ensure that exploitation is conducted at a minimal level in such cases (FAO, 2000). This is particularly the case for sharks, given their generally low productivity and vulnerability to overfishing. The FAO guidelines also emphasize the need for specialist training, species identification guides and catalogues, and shared databases for transboundary species. A significant step was made with the publication of a technical manual for shark fisheries management, funded by the Asian Pacific Economic Cooperation (APEC; Musick and Bonfil, 2004). This manual provides guidance to shark-fishing States in data collection, monitoring, and management, and in implementation of the IPOA-Sharks. Yet a concerted effort is required to streamline the process through a regular program of regional training and capacity-building workshops in those States requiring such assistance, facilitated by experts in shark fishery monitoring and management. As an example, Australia, whose NPOA appears to meet the standards recommended by FAO (Anonymous, 2004c), is well positioned to assist other States in developing their NPOAs. Indeed, through an ongoing Australian Centre for International Agricultural Research project on shark and ray fisheries in eastern Indonesia, Australian experts have been helping Indonesia develop aspects of their NPOA. The program includes technical training for Indonesian partners to enhance the country’s stock-assessment capability (www.aciar.gov.au).

Lack of resources Despite the high value of their fins, sharks remain a low priority relative to other commercial species in terms of allocation of often-scarce human and financial resources in fisheries departments. The issue of funding was identified as a major constraint by all developing States responding to FAO’s call for information on progress in 2003. Several States have approached FAO for technical and financial assistance (Cochrane, 2003), and Paragraph 30 of the IPOA states that FAO will “support development and implementation of Shark Plans … with Regular Programme funds and by use of extrabudgetary

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funds made available for this purpose.” At the time of writing, only Japan and the United States are known to have provided funds to support implementation by other States. At the APEC Fisheries Working Group Workshop on Sharks in December 2002, the decision was made to develop a program to assist States with the IPOA-Sharks development and implementation, but there has been little or no progress since then. The national members of the West African Sub-Regional Commission on Fisheries have placed great importance on the implementation of the IPOA-Sharks with financial support from an environmental foundation active in the region, as well as assistance from the IUCN SSG (which, as a voluntary network, is unable to meet all requests for assistance). Ensuring that these and other States’ initial efforts are translated into improved long-term data collection, monitoring, and management may require additional financial and capacitybuilding assistance from developed States, FAO, and other sources. There are, however, so many shark-fishing States requiring assistance that it will be necessary to carefully target the limited financial and staff resources to the regions with the greatest need. These may include those with the largest shark fisheries, the greatest dependence on sustainably managed fisheries resources (particularly from shared stocks), and/or the highest shark biodiversity. Ideally, a more structured long-term strategy should be developed to deliver improved shark fisheries management in these areas.

Pelagic sharks and the IPOA Relatively little is known about pelagic shark stock structure and interactions, although recent studies have found that some species of pelagic sharks (Baum et al., 2003; Baum and Myers, 2004; ICCAT, 2005), including porbeagles (Lamna nasus) (DFO, 2001; Campana et al., 2008), shortfin makos (Babcock and Nakano, 2008), and possibly even the relatively prolific blue sharks (Hueter and Simpfendorfer, 2008), have undergone significant declines under fishing pressure (Camhi, 2008). With regard to pelagic sharks, the lack of a basic understanding of the structure of most stocks, the poor quality of recorded “bycatch” data, and uncertainty surrounding the sustainability of current levels of fishing are significant issues. Furthermore, management constraints are compounded because the oceanic and migratory habits of pelagic sharks often result in wide ranges, large parts of which fall outside the responsibility of individual countries, and outside the mandate of various international bodies (Weber and Fordham, 1997; Stevens and Wayte, 1999). Individual fishing States should adopt a precautionary approach by undertaking research, management, and protection for pelagic sharks within their own waters, but cooperative regional and international efforts are imperative for these measures to be effective. FAO has recognized the importance of cooperation and coordination regarding NPOAs (FAO, 2000; Pawson and Fowler, 2001), and international collaboration on data collection and data-sharing systems for stock assessment is particularly important (Stevens and Wayte, 1999). The IPOA-Sharks guidelines emphasize the need for regional plans where appropriate (FAO, 2000), and these are especially critical for multinational, multispecies fisheries taking pelagic sharks in international waters. RFOs are responsible for the management of multinational fisheries in international waters that take large numbers of pelagic sharks as bycatch. To date, no RFO has drafted

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or implemented a Shark Plan as suggested in the FAO Technical Guidelines (FAO, 2000) to help coordinate management efforts among member fishing States. In November 2004, however, the International Commission for the Conservation of Atlantic Tunas (ICCAT) adopted by consensus a binding Recommendation (04-10) that requires Member States to report shark catches and to limit fins to 5% of the weight of sharks onboard up to the point of first landing (the latter restriction is aimed at ending the practice of shark finning in ICCAT fisheries) (ICCAT, 2004; Babcock and Nakano, 2008). The ICCAT measure also encourages release of live sharks and research into gear selectivity (to reduce shark bycatch) and pelagic shark nursery grounds. In 2005, similar finning bans were adopted by the Inter-American Tropical Tuna Commission (IATTC) in the eastern tropical Pacific and by the Indian Ocean Tuna Commission (IOTC) for its fisheries in the Indian Ocean. The Convention on the Conservation of Antarctic Marine Living Resources (CCAMLR) adopted a measure (32-18) in 2006 that prohibits directed fishing for sharks in the Convention area until it can assess the impacts of such fishing. Although some RFOs are beginning to call for species-specific reporting of shark landings, which are critical to the development of effective management plans, few fishing States have done so (Camhi et al., 2008b). As no other substantive action on behalf of sharks is being taken by the RFOs, pelagic sharks are largely without management in most oceans of the world (Camhi et al., 2008a).

Summary Serious concern regarding the slow progress toward implementation of the IPOA-Sharks since its adoption in 1999 has been voiced repeatedly by FAO, CITES, IUCN, TRAFFIC, the UN General Assembly, many individual States, and conservation NGOs. There has been very little improvement in the collection of catch and trade data, or in conservation and management. This situation has arisen because of a lack of political will, technical capacity, and human and financial resources, and because the IPOA-Sharks is wholly voluntary. States and RFOs are not obliged to undertake any of the actions urged by FAO in the IPOA, and it appears that few consider it to be a priority. Even so, as noted by the United States when urging other States to complete their NPOAs, this would only be the first step toward comprehensive shark fisheries management at national, regional, and global levels (Pawson and Fowler, 2001). Since the passage of the IPOA-Sharks, we have learned a great deal about the vulnerability of pelagic sharks, as evidenced by serious declines in numerous populations (e.g., Baum et al., 2003; Baum and Myers, 2004; Camhi, 2008). Though there is little doubt that the existence of the voluntary IPOA-Sharks has raised the awareness of the conservation and management needs of this vulnerable group of fishes on an international level, it is too early to evaluate the extent to which its implementation will lead to actual improvement in the status of shark populations. It is vital not to lose sight of the overall aims of the IPOASharks: to improve species-specific shark catches, landings, and trade information, and to strengthen the monitoring and management of shark fisheries. Simply going through the motions of drafting an NPOA, but failing to identify and commit to specific management actions and frequent review of the situation, does little to strengthen the conservation and management of shark populations.

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Given the jurisdictional complications in the management of oceanic migrants, pelagic sharks – particularly those whose populations are known to already be seriously depleted or likely declining steeply – should rank among the highest priorities for conservationists, scientists, and international fisheries management bodies.

Acknowledgments The authors thank all the members of the IUCN SSG who have provided information to assist us in monitoring progress with the IPOA-Sharks. We also thank Glenn Sant and Anna Willock (TRAFFIC International), Kevern Cochrane and Ross Shotton (FAO Fisheries Department), Tom de Meulenear and Rod Hay (CITES Secretariat and Animals Committee, respectively), and Emma Montgomerie for their assistance, and Claudine Gibson (IUCN SSG), Susie Watts, and Sonja Fordham (The Ocean Conservancy) for helpful comments on the manuscript.

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FAO (2005) Progress in the Implementation of the Code of Conduct for Responsible Fisheries and Related International Plans of Action. Report of the Twenty-sixth Session of the Committee on Fisheries, Rome, 7–11 March 2005. COFI/2005/2. FAO, Rome, Italy, 15 pp. FAO (2006) Report of the FAO Expert Consultation on the Implementation of the FAO International Plan of Action for the Conservation and Management of Sharks. FAO Fisheries Report No. 795. FAO, Rome, Italy, 24 pp. Fowler, S., Mogonsen, C. B. and Balsdale, T. (2004) Plan of Action for the Conservation and Management of Sharks in UK Waters. Joint Nature Conservation Committee, Peterborough, UK, 66 pp. www.fao.org/figis/servlet/static?xml⫽ipoa_sharks.xml&dom⫽org&xp_nav⫽3, accessed 28 January 2007. Fowler, S. L. and Cavanagh, R. D. (2005) International conservation and management initiatives for chondrichthyan fish. In: Sharks, Rays and Chimaeras: The Status of the Chondrichthyan Fishes (eds. S. L. Fowler et al.). IUCN/SSC Shark Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp. 58–69. Government of Japan (2001) Japan’s National Plan of Action for the Conservation and Management of Sharks, 7 pp. www.fao.org/figis/servlet/static?xml⫽ipoa_sharks.xml&dom⫽org&xp_nav⫽3, accessed 28 January 2007. Hueter, R. E. and Simpfendorfer, C. A. (2008) Case study: Trends in blue shark abundance in the western North Atlantic as determined by a fishery-independent survey. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. ICCAT (2004) Recommendation by ICCAT Concerning the Conservation of Sharks Caught in Association with Fisheries Managed by ICCAT. BYC 04-10. www.iccat.es/Documents/Recs/ compendiopdf-e/2004-10-e.pdf, accessed 28 January 2007. ICCAT (2005) Report of the 2004 Inter-sessional Meeting of the ICCAT Sub-committee on By-catches: Shark Stock Assessment, Tokyo, Japan, 14–18 June 2004. ICCAT Collective Volume of Scientific Papers 58(3), 799–890. IUCN/SSC Shark Specialist Group and TRAFFIC (2002a) Report on Implementation of the International Plan of Action for Sharks (IPOA-Sharks). AC18 Doc. 19.2. Eighteenth Meeting of the CITES Animals Committee, San José, Costa Rica, 8–12 April 2002. www.cites.org/eng/com/ ac/18/E18-19-2.pdf, accessed 28 January 2007. IUCN/SSC Shark Specialist Group and TRAFFIC (2002b) The Role of CITES in the Conservation and Management of Sharks. www.cites.org/common/notif/2002/ESF042A.pdf, accessed 28 January 2007. Kohler, N. E. and Turner, P. A. (2008) Stock structure of the blue shark, Prionace glauca, in the North Atlantic Ocean based on tagging data. In: Sharks of the Open Ocean: Biology, Fisheries and Conservation (eds. M. D. Camhi, E. K. Pikitch and E. A. Babcock). Blackwell Publishing, Oxford, UK. Lack, M. and Sant, G. (2006) Confronting Shark Conservation Head On! TRAFFIC International, Cambridge, UK, 29 pp. Lucas, V. and Gamblin, C. (2006) Seychelles National Plan of Action for the Conservation and Management of Sharks: An update on the status. www.iotc.org/files/proceedings/2006/wpby/ IOTC-2006-WPBy-10.pdf, accessed 28 January 2007. Malaysia Department of Fisheries (2005) Malaysia National Plan of Action for the Conservation and Management of Shark (Draft). Department of Fisheries, Kuala Lumpur, Malaysia, 57 pp. www.fao .org/figis/servlet/static?xml⫽ipoa_sharks.xml&dom⫽org&xp_nav⫽3, accessed 28 January 2007. Musick, J. A. (1999) Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals. American Fisheries Society, Bethesda, MD.

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Musick, J. A. and Bonfil, R. (2004) Elasmobranch Fisheries Management Techniques. Asian Pacific Economic Cooperation Secretariat, Singapore. www.flmnh.ufl.edu/fish/organizations/ssg/ EFMT2004.htm, accessed 28 January 2007. Nageon de Lestang, J. (1999) Management of shark fisheries in Seychelles. In: Case Studies of the Management of Elasmobranch Fisheries (ed. R. Shotton). FAO Fisheries Technical Paper. No. 378/1. FAO, Rome, Italy, pp. 284–315. Nevill, J., Robinson, J., Giroux, F. and Isidore, M. (2007) Seychelles National Plan of Action for the Conservation and Management of Sharks-Draft. Seychelles Fishing Authority, Mahé, Republic of Seychelles, 58 pp. NMFS (2001) Final United States National Plan of Action for the Conservation and Management of Sharks. NOAA/NMFS, Silver Spring, MD, 90 pp. www.nmfs.noaa.gov/sfa/hms/Final%20NPOA .February.2001.htm, accessed 28 January 2007. Pawson, M. and Fowler, S. L. (2001) International shark conservation and management initiatives. Shark News. The Newsletter of the IUCN Shark Specialist Group 13, 13. SEAFDEC (2006) Report on the Study of Shark Production, Utilization and Management in the ASEAN Region 2003–2004. Southeast Fisheries Development Center, Bangkok, Thailand, 229 pp. Shark Advisory Group and Lack, M. (2004) National Plan of Action for the Conservation and Management of Sharks (Shark-Plan). Department of Agriculture, Fisheries and Forestry, Canberra, Australian Capital Territory, Australia, 82 pp. www.daffa.gov.au/fisheries/environment/bycatch/ sharkplan, accessed 28 January 2007. Stevens, J. D. and Wayte, S. E. (1999) A Review of Australia’s Pelagic Shark Resources. Final Report to the Fisheries Research and Development Corporation, Project 98/107. CSIRO Marine Research, Hobart, Tasmania, Australia, 64 pp. Taiwan Fisheries Agency (2006) Taiwan’s National Plan of Action for the Conservation and Management of Sharks. Fisheries Agency, Taipei, Taiwan. www.fa.gov.tw/eng/guide/npoasharke .php, accessed 28 January 2007. UN General Assembly (2005) Sustainable fisheries, including through the 1995 Agreement for the Implementation of the Provisions of the United Nations Convention on the Law of the Sea of 10 December 1982 relating to the Conservation and Management of Straddling Fish Stocks and Highly Migratory Fish Stocks, and related instruments. A/RES/58/14 (2003), A/RES/59/25 (2004), and A/RES/60/31 (2005). www.un.org/depts/los/general_assembly/general_assembly_ resolutions.htm, accessed 28 January 2007. Walker, T. I. (1998) Introduction: Shark fisheries management and biology. Marine and Freshwater Research 49(7), iii. Weber, M. L. and Fordham, S. V. (1997) Managing Shark Fisheries: Opportunities for International Conservation. TRAFFIC International and the Center for Marine Conservation, Washington, DC.

Index

Note: Page numbers in italics refer to figures or tables. abundance catch-rate data and, 6, 7, 164–65, 205–11, 213, 214, 237, 356 decline in, xxiv generalized linear model to derive indices of, 205 population dynamics models and, 6 Alaska, 101, 182, 199–200 pelagic longline experiment in, 462–68 salmon shark and, 95–101, 99, 433 albacore tuna (Thunnus alalunga), 260, 300 Alopiidae. See bigeye thresher (Alopias superciliosus); common thresher (A. vulpinus); pelagic thresher (A. pelagicus) American Samoa, 269 angel shark. (Squatina californica) intrinsic rates of increase for, 289 productivity of, 293 rebound potential of, 291 angling. See fisheries, recreational Argentina, 339, 370 commercial fisheries of, 172, 177, 182–83, 186 management in, 426, 434 NPOA development in, 482, 484 artificial bait, 464–65 Atlantic Ocean, xxv commercial fisheries in, 172–74, 175, 177, 213–26, 260–67, 403–4, 435 recreational fisheries in, 205–11 management in, 420–37, 482–83, 488 shark finning bans in, 8, 421–22 See also catch rates (CPUE) and trends Atlantic sharpnose (Rhizoprionodon terraenovae), 289 productivity of, 293 rebound potential of, 292, 300 Atlantic stingray (Dasyatis sabina), 158 Australia, 33 commercial fisheries of, 65, 177, 260–67, 427 Endangered Species Protection Act (1997) of, 405 management in, 424, 427, 433, 434, 435 NPOA development in, 481, 482, 484, 486 recreational fisheries in, 193, 194, 196–97, 399 school shark in, 369–85 shark finning and, 8, 9, 421, 423, 435 Australian sharpnose (Rhizoprionodon taylori), 289 Azores, 163, 370 recreational fisheries in, 193, 201 swordfish longline fisheries in, 230–34 Azores dogfish (Scymnodalatias garricki), 19 Bahamas, 201 Barcelona Convention, 424, 431, 437 basking shark (Cetorhinus maximus), 16, 21 biology and ecology of, 17 intrinsic rates of increase for, 288 management of, 42 productivity of, 292, 293, 293 rebound potential of, 291, 292

wildlife conservation agreements and, 432 batoids (skates and rays), 14, 15, 15, 20 Bayesian methods, 286, 351, 359–64 benthic sharks, 14 Bering Sea, 101 Bermuda: recreational fisheries in, 201 Beverton–Holt stock recruitment model, 301, 302 bigeye sand tiger shark (Odontaspis noronhai), 16, 17 bigeye thresher shark (Alopias superciliosus), 5 abundance of, 395 age and growth of, 62–64, 62, 163, 168 biology and ecology of, 15, 16, 17, 60–65 catch rates (CPUE) and trends for, 402, 403 commercial fisheries and, 7, 65, 163, 167, 168, 171, 177–78, 214, 215, 221, 242, 243, 244, 245, 250, 251, 261, 269, 276, 465 conservation status of, 397, 399, 401, 402, 411 diet of, 21, 64–65 distribution of, 57, 60–61 fecundity of, 309 genetic population structure of, 326 ICCAT data collection on, 473 life-history parameters of, 311, 312, 314, 317 litter size, 28 management and, 65, 272, 424, 432, 433, 434 movements of, 61 productivity of, 285, 292, 293, 293, 309, 398 rebound potential of, 285, 291, 292 recreational fisheries and, 193, 194, 198–200 reproduction in, 24, 28, 29, 30, 32, 32, 34, 35, 58, 64 segregation by sex and age of, 63 species protections and, 424 stock structure of, 62 wildlife conservation agreements and, 432 bigeye tuna (Thunnus obesus), 300, 465 bignose shark (Carcharhinus altimus), 17 biodiversity. See diversity of pelagic elasmobranchs blacknose shark (Carcharhinus acronotus), 329 blacktip shark (Carcharhinus limbatus) biology and ecology of, 18 fisheries and, 222, 276 genetic population structure of, 328, 329 intrinsic rates of increase for, 289, 362 productivity of, 293 rebound potential of, 292 stock assessment of, 361 blue marlin (Makaira nigricans), 300, 304, 466 blue shark (Prionace glauca), 5 abundance of, 128–29, 153, 236–40, 339 age and growth of, 133, 141, 142 biology and ecology of, 15, 18, 140–48 as bycatch, 4, 340 catch rates (CPUE) and trends for, 7, 147, 164–65, 185, 205–11, 208, 210, 218, 220, 222, 223, 224, 230–33, 231, 232, 233, 236–40, 239, 250, 251, 254, 260, 262–63, 264, 265, 266, 268–71, 270, 404, 408–9, 465, 473–77

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Index

blue shark (Prionace glauca) (Contd.) commercial fisheries and, 7, 141, 145–47, 163, 167, 168, 171, 172, 173, 173, 174, 176, 177–78, 213, 214, 215, 221, 223–25, 230–34, 236–40, 239, 242, 244, 245, 247, 250–51, 251, 254, 260–67, 261, 264, 265, 266, 269, 276, 279, 340 conservation status of, 147–48, 267, 271, 399, 400, 401, 408–9, 409–10 demographic analysis of, 133 diet of, 21, 140–48, 142–43 distribution of, 57, 140–48, 236, 339, 341–42, 408 fecundity of, 236, 309 genetic population structure of, 326 ICCAT assessment of, 473, 474–76 life-history parameters of, 309, 311, 312, 314, 340 management and, 272, 420, 424, 435, 436 movements of, 3, 90, 117, 140–48, 143–45, 144, 146, 286, 339–40, 341–42, 342–47, 373 population assessment of, 140–48, 408 productivity of, 293, 309, 398, 408 rebound potential of, 291, 300, 306 recreational fisheries and, 164, 193, 194, 196, 197, 198, 199, 200, 205–11 reproduction in, 24, 29, 32, 35, 38, 39, 40–41, 58, 140–48 segregation by sex and age of, 57, 140–48, 286, 347 species protections and, 424 stock assessment of, 340, 395, 400 stock structure of, 57, 286, 339–48 tagging studies of, 57, 140–48, 286, 339–48 bluefin tuna (Thunnus thynnus), 300, 304, 465 bluntnose sixgill shark (Hexanchus griseus), 18 bluntnose stingray (Dasyatis sayi), 158 Bonn Convention (CMS), 432–33 bonnethead shark (Sphyrna tiburo) intrinsic rates of increase for, 289 rebound potential of, 292, 300 Brazil, 163 commercial fisheries of, 165, 166, 168, 172, 173, 177, 179, 186, 214, 216, 217, 218, 219–21, 222, 224 management in, 426, 434 NPOA development in, 482 shark finning and, 8, 171, 421, 423 broadband lanternshark (Etmopterus gracilispinis), 18–19 bronze whaler shark (Carcharhinus brachyurus), 17 Australian tuna longline fisheries and, 261, 261 brown smoothhound shark (Mustelus henlei) productivity of, 293 rebound rates of, 291 Brunei Darussalam: NPOA development in, 482, 484 bull shark (Carcharhinus leucas), 18 Mexican Pacific fisheries and, 276 productivity of, 293 rebound potential of, 292, 300 California sardine (Sardinops sagax): rebound potential of, 303 Cambodia: NPOA development in, 482, 484 Canada, 408 commercial fisheries of, 172, 177, 183, 186 catch-rate data and, 173, 185 finning prohibitions in, 8, 421, 423 management in, 427, 433, 434, 435, 447–48 NPOA development in, 482 recreational fisheries in, 200–201 Canary Islands, 347 Cape Verde Islands, 347 finning prohibitions in, 421 NPOA development in, 482, 484 Carcharhinidae (requiem sharks), 17–18 See bignose shark (Carcharhinus altimus); blacktip shark (C. limbatus); blue shark (Prionace glauca); bronze whaler shark (C. brachyurus); bull shark (C. leucas); dusky shark (C. obscurus); Galapagos shark (C. galapagensis); night shark (C. signatus); oceanic

whitetip shark (C. longimanus); sandbar shark (C. plumbeus); silky shark (C. falciformis); silvertip shark (C. albimarginatus); spinner shark (C. brevipinna); tiger shark (Galeocerdo cuvier) Carcharhiniformes, 14, 15, 15, 17–18 Caribbean: recreational fisheries in, 193, 194 carpet sharks (Orectolobiformes), 14, 15, 16 cartilaginous fishes (chondrichthyans), 3, 5, 14, 15, 17 catch and landings. See fisheries, commercial; fisheries, recreational; country names; shark names catch rates (CPUE) and trends abundance and, 6, 7, 164–65, 205–11, 213, 214, 237, 356 Atlantic Ocean fisheries and, 172–74, 210, 211, 213, 218–23, 220, 222, 224, 230–33, 231, 232, 236–40, 239, 473–77 conservation status and, 7, 163, 400–409, 403–4 gaps and limitations in data on, xxv, 6–7, 10, 166–70, 209–10 generalized linear model and, 164 Indian Ocean fisheries and, 252, 255 management and, 165, 167–68, 469–70, 473–77 Pacific Ocean fisheries and, 260–67, 268–72, 270, 271, 278–79, 374–75 recreational, 205–211, 209, 210 stock assessment and, 355–56 See also shark names CCAMLR. See Commission for the Conservation of Antarctic Marine Living Resources CCSBT. See Commission for the Conservation of Southern Bluefin Tuna Cetorhinidae. See basking shark (Cetorhinus maximus) Chile: NPOA development in, 482 Chimaeriformes, 15 China commercial fisheries of, 177, 214, 215 management in, 434 Chlamydoselachidae (frilled sharks), 18 CITES. See Convention on International Trade in Endangered Species of Wild Fauna and Flora CMS (Bonn Convention), 432–33 coastal sharks open ocean sharks vs., 14 reproduction in, 27 research and, 6–8 See also shark names Code of Conduct for Responsible Fisheries, 425, 480 collapse threshold, 302, 305, 306 Colombia: NPOA development in, 482 Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR), 428, 429, 488 Commission for the Conservation of Southern Bluefin Tuna (CCSBT), 426–27, 429 Committee on the Status of Endangered Wildlife in Canada (COSEWIC), 406, 425 common thresher shark (Alopias vulpinus), 5 abundance of, 153, 395 age and growth of, 60, 62–64, 62 biology and ecology of, 15, 16, 17, 60–65 birth size and, 63 catch rates (CPUE) and trends for, 7, 268–71, 270, 402, 403 commercial fisheries and, 7, 65, 167, 167, 168, 171, 176, 177–78, 214, 250, 251, 261, 276 conservation status of, 65, 397, 399, 401, 402, 405, 411 demographic analysis of, 133, 133 diet of, 21, 64–65 distribution of, 57, 60–61 fecundity of, 309 genetic population structure of, 326, 328 ICCAT data collection on, 473 life-history parameters of, 309, 311, 312, 317 longevity of, 63 management and, 65, 272, 424, 432, 433, 435 movements of, 57, 61 productivity of, 65, 293, 309, 398 rebound potential of, 291, 300, 303

Index

recreational fisheries and, 65, 193, 194, 198, 199, 200 reproduction in, 24, 28, 29, 30, 32–33, 32, 34, 35, 58, 64 segregation by sex and age of, 63 sexual maturity of, 60 species protections and, 424 stock structure of, 62 wildlife conservation agreements and, 432 conservation beach protection programs and, 399 bycatch data reporting and, 400 comparative life history and, 309, 316–18 data constraints and, 6 genetic population structure and, 323 Indian Ocean fisheries and, 254–55 stock assessment and, 351 See also management conservation status, 5–8, 58, 397–411 catch rates and, 400–409, 403–4, See also shark names Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), xxiv, 76, 168, 169, 186, 398, 405, 424, 426, 430, 431–32, 439, 472, 479–80, 481–83, 488 cookiecutter or cigar shark (Isistius brasiliensis), 19, 21, 215 fisheries and, 214 ICCAT data collection on, 473 Cooperative Shark Tagging Program, 117, 131, 198, 199, 237, 339, 340 COSEWIC. See Committee on the Status of Endangered Wildlife in Canada Costa Rica: shark finning and, 8, 171, 421, 423 Croatia, 436 crocodile shark (Pseudocarcharias kamoharai), 15, 16, 17, 21 fisheries and, 214, 215, 261, 261 ICCAT data collection on, 473 Cuba: commercial fisheries of, 177 Cyprus: commercial fisheries of, 177 Dalatiidae (kitefin sharks), 19 Dasyatidae. See pelagic stingray (Pteroplatytrygon violacea) demographic analysis, xxv age-specific mortality and, 285 Bayesian methods and, 351, 359–64 comparative life history and, 309–19 density dependence and, 133, 285, 310 fecundity and, 6, 285 fishing mortality and, 6 inaccurate data and, 285 intrinsic rates of increase and, 288–94 life-history parameters and, 291–92, 309–19, 361 matrix population model and, 310 maximum sustainable yield and, 133 Monte Carlo simulation and, 310 natural mortality and, 6 population and, 285, 310, 354 productivity and, 285 rebound potential and, 298 stock assessment and, 352, 354 Denmark, 173 devilray, 15, 21 diamond stingray (Dasyatis dipterura), 158 dogfish sharks (Squaliformes), 261 dolphinfish (Coryphaena hippurus), 465 dusky shark (Carcharhinus obscurus), 6, 18 fisheries and, 222, 242, 243, 244, 245, 261, 276, 465 intrinsic rates of increase for, 289 productivity of, 293, 398 rebound potential of, 292, 304 species identification of tissues of, 334, 335, 336 ecomorphotypes, 14, 15 Ecuador, 425 management in, 434

495

NPOA development in, 482, 484 shark finning and, 8, 421 Egypt, 425 shark finning and, 8, 421 elasticity analysis, 309–319, 316 El Salvador: finning prohibitions in, 421 Etmopteridae (lanternsharks), 18–19 Euler–Lotka equation, 288–89, 298, 299, 313 European Union (EU), 396, 419, 432 management and, 436 NPOA development and, 481, 482, 484 shark finning and, 8, 420, 422, 423 extinction, 7, 10 FAO. See Food and Agriculture Organization Faroe Islands, 173, 446 fecundity, 57, 58 demographic analysis and, 6, 285 rebound potential and, 299, 301 Fiji, 177 finning. See shark finning fisheries agreements international treaties, 425–28 IPOA–Sharks and, 8, 168, 186, 396, 418, 419, 425, 430 RFMOs and, 428–30 wildlife conservation agreements, 430–33 fisheries, commercial 166–186, 177–78 artisanal, 276–77 Atlantic Ocean, 171, 172–74, 179, 181, 182, 183, 184, 185, 205–11, 213–26 billfish, 90 blue shark and, 145–47 bycatch mortality reduction in, 462–70 catch-rate data and, 163–65, 167–70 conservation status and, 58, 398–99 discard data and, xxiv, xxv, 214 expansion of, 419 gill-net, 87, 90, 277–78 global overview of, 166–86 handline, 268 Indian Ocean, 171, 175–76, 181, 183, 194, 247–55 management of, 6, 418–39 Mexican Pacific, 275–81 Pacific Ocean, 171, 174–75, 175, 179, 180, 181, 182, 183, 184 pole and line, 268 purse-seine, 269 shark fin trade and, 167, 171, sustainability of, 4–8 swordfish longline, 4, 230–34 tuna, xxiv, 4, 90 utilization and, 135–36 See also longline fisheries; fisheries, recreational; country names fisheries management. See management fisheries, recreational, 10, 65, 90–91, 163, 184, 195, 196, 240, 341, 399, 434 Australia, 193, 194, 196–97 bigeye thresher and, 193, 194, 198, 199, 200 blue shark and, 193, 194, 196, 197, 198, 199, 200, 205–11 Canada, 200–201 catch-and-release fishing and, 196–97 common thresher and, 193, 194, 198, 199, 200 conservation status and, 399 information sources for, 194 Ireland, 193, 200 Italy, 193, 194 longfin mako and, 196, 199, 200, 205–11 mortality rates and, 201–2, 399 New Zealand, 193, 193–202, 194 night shark and, 199 oceanic whitetip shark and, 198, 199 pelagic thresher and, 193, 194, 198, 200 porbeagle and, 193, 196, 200

496

Index

fisheries, recreational (Contd.) salmon shark and, 193 shark tournaments and, 197, 205–9, 399 shortfin mako and, 193, 194, 196, 198, 199, 200, 205–11 silky shark and, 198 South Africa, 193, 194, 201 tagging studies and, 193, 197 United Kingdom, 193, 194, 200 United States, 193, 194, 198–200, 205–11 white shark and, 194, 196 Food and Agriculture Organization (FAO), 100, 214, 400–401, 419 catch data and, 163, 166, 168, 175, 176, 185, 186 Code of Conduct for Responsible Fisheries of, 425, 480 Committee of Fisheries (COFI) of, 478, 480 data collection and, 472–73 finning prohibitions in, 421 IPOA–Sharks and, 8, 168, 186, 396, 418, 419, 425, 430, 446, 478–89 management and, 396 Plan of Action for Sharks in the Indian Ocean of, 247 food web structure, 4, 8 Fowler’s regression equation, 319 France commercial fisheries of, 172, 173, 177, 183, 186 management in, 426, 434 NPOA development in, 482, 484 French Polynesia: finning prohibitions in, 422 frilled shark (Chlamydoselachus anguineus), 18 Galapagos shark (Carcharhinus galapagensis), 18 catch rates for, 269 productivity of, 293 rebound potential of, 291–92 Gambia, The: NPOA development in, 483, 484 General Fisheries Commission of the Mediterranean (GFCM), 429 management for sharks and, 421, 429 membership in, 426–27 shark finning and, 8, 421 genetic analysis conservation and, 323 molecular markers, 325–28 species identification of pelagic shark tissues and, 334–37, 335, 336, 337 stock structure and, 72, 323–30 tagging studies vs., 323 Germany, 177 GFCM. See General Fisheries Commission of the Mediterranean Ginglymostomatidae, 16 goblin shark (Mitsukurina owstoni), 16, 17 gray reef shark (Carcharhinus amblyrhynchos), 291, 293 gray smoothhound shark (Mustelus californicus), 291, 293, 300 Greece: commercial fisheries of, 177 ground sharks (Carcharhiniformes), 17–18 Guam: commercial fisheries of, 269 Guinea: NPOA development in, 482, 484 Guinea-Bissau: NPOA development in, 482, 484 Gulf of Alaska, 101 pelagic longline experiment in, 464–65, 467–68 Gulf of Mexico, 7, 33 pelagic longline experiment in, 463–64, 465–67 hammerhead sharks (Sphyrnidae). See scalloped hammerhead (Sphyrna lewini) Hawaii, 17, 200 catches from, 269, 270, 271 management in, 268–73 white shark in, 70, 84 Hexanchidae (sixgill and sevengill sharks), 18 Hexanchiformes (cow and frilled sharks), 14, 15, 17–18, 18 Highly Migratory Species Fisheries Management Plan, 65, 199

IATTC. See Inter-American Tropical Tuna Commission ICCAT. See International Commission on the Conservation of Atlantic Tunas ICES. See International Council for the Exploration of the Sea IGFA. See International Game Fish Association India commercial fisheries of, 172, 176, 177, 183, 186 management in, 426, 434, 436 NPOA development in, 482 shark bycatch of, 247, 250 shark finning and, 171 Indian Ocean commercial fisheries in, 110, 123, 134–35, 147, 170, 175–76, 181, 183, 184, 186, 247–55, 402 management in, 420–37, 482–83, 488 recreational fisheries in, 194 shark finning bans in, 8, 421–22 See also catch rates (CPUE) and trends; country names Indian Ocean Tuna Commission (IOTC), 169, 176, 247, 429 IPOA–Sharks implementation and, 488 management for sharks and, 8, 176, 185, 254–55, 429 membership in, 426–27 shark bycatch and, 169, 176, 248–54, 249, 250, 428 shark finning and, 8, 9, 421, 429 Indo-Pacific sailfish (Istiophorus platypterus), 300, 466 Indonesia commercial fisheries of, 166, 172, 176, 177, 179, 186 management in, 426, 434, 436 NPOA development in, 482, 484 recreational fisheries in, 201 shark bycatch of, 248 shark finning and, 171 Inter-American Tropical Tuna Commission (IATTC), 395, 421, 428, 429, 488 management for sharks and, 124, 426, 428, 429 shark bycatch and, 169, 174, 175 shark finning and, 8, 9, 421, 429, 488 International Commission on the Conservation of Atlantic Tunas (ICCAT), 124, 136, 147, 169, 172, 174, 214, 216, 429, 472–77, 488 assessment efforts of, 400, 472, 474–76 blue shark and, 474 commercial fisheries of, 186 conservation and, 395 data collection and, 472–74 management for sharks and, 421, 429, 474 membership in, 426–27 shark finning and, 8, 9, 421, 423, 429 shortfin mako and, 91, 474 International Council for the Exploration of the Sea (ICES), 169, 430 International Game Fish Association (IGFA), 193, 194, 198 International Pelagic Shark Workshop, xxiv, 4, 5–6 International Plan of Action for the Conservation and Management of Sharks (IPOA–Sharks), 8, 168, 186, 247, 396, 418, 419, 425, 430, 446, 478–89 CITES and, 479–80 implementation of, 481–87 IUCN and, 478 pelagic sharks and, 487–88 progress of, 479, 483–85, 482–483 RFMOs and, 487–88 See also country names international treaties, 425–28 CITES, xxiv, 76, 168, 169, 186, 398, 405, 424, 426, 430, 431–32, 439, 472, 479–80, 481–83, 488 Code of Conduct for Responsible Fisheries, 425 IPOA–Sharks, 8, 168, 186, 396, 418, 419, 425, 430, 446, 478–89 membership to, 426–27 UN Convention on the Law of the Sea (UNCLOS), 425, 428, 437, 438 UN Driftnet Ban, 425 UN Fish and Stocks Agreement (UNFSA), 425, 428, 438

Index

IPOA–Sharks. See International Plan of Action for the Conservation and Management of Sharks Iran: management in, 427, 434 Ireland, 177, 193, 200, 347, 399 Israel, 425 shark finning and, 8, 422 Italy commercial fisheries of, 177 NPOA development in, 481, 482 recreational fisheries in, 193, 194, 201 IUCN. See World Conservation Union Japan commercial fisheries of, 166, 172, 173, 177, 179–80, 185, 186, 214, 215 management in, 426, 434, 436 NPOA development in, 481, 482, 484, 487 shark bycatch of, 248–49, 250 shark finning and, 171 Jaws, 198 Kenya commercial fisheries of, 177 recreational fisheries in, 201 Korea, Republic of commercial fisheries of, 166, 172, 177, 180–81, 186, 214, 216 management in, 427, 434, 436 NPOA development in, 482 Lamnidae (mackerel sharks) See longfin mako (Isurus paucus); porbeagle (Lamna nasus); salmon shark (L. ditropis); shortfin mako (I. oxyrinchus); white shark (Carcharodon carcharias) Lamniformes (mackerel sharks), 14, 15, 15, 16, 17, 28–37, 60, 251 lanternsharks (Etmopteridae), 18–19 large coastal sharks, 361–63 largetooth cookiecutter shark (Isistius plutodus), 19 lemon shark (Negaprion brevirostris) genetic population structure of, 329 intrinsic rates of increase for, 289 productivity of, 293 rebound potential of, 292 leopard shark (Triakis semifasciata) productivity of, 293 rebound potential of, 291, 300, 306 life-history parameters, 312, 314, 315, 316 age and growth, 309, 311, 313 body size, 309, 310 demographic analysis and, 291–92, 309–19, 361 exploitation and, 310 fecundity, 310, 313; See also litter size intrinsic rates of increase for, 291–92 mortality and, 285 offspring length, 310 population and, 309, 310, 316–19 principal component analysis (PCA) of, 310–11 reproduction, 309 von Bertalanffy growth equation and, 60 litter size, 3, 25, 27, 312, 313 in lamniform sharks, 28–30, 29, 58, 64, 69, 74–75, 87, 88, 89, 97, 105, 108, 110 in pelagic stingray, 41, 152, 155, 158 in requiem sharks, 37–38, 114, 119, 131–32, 141, 237, 316 See also shark names longfin mako (Isurus paucus), 5 biology and ecology of, 15, 17 catch in longline fisheries, 465 catch rates (CPUE) and trends for, 250, 252–53, 403, 406 commercial fisheries and, 163, 167, 168, 171, 173, 176, 177–78, 214, 215, 261 conservation status of, 397, 401, 406, 411 ICCAT data collection on, 473, 474

497

management and, 272, 424, 432, 433, 434 rebound potential of, 300 recreational fisheries and, 196, 199, 200, 205–11 reproduction in, 24, 28, 29, 31, 32, 35, 36, 58 species identification of tissues of, 334, 335, 336 species protections and, 424 wildlife conservation agreements and, 432 longline fisheries, 87, 90, 268, 277, 462–70 bycatch mortality reduction in, 462–70 catch data for, 465 Gulf of Alaska experiment and, 464–65, 467–68 Gulf of Mexico experiment and, 463–64, 465–67 shark bycatch in, 242–45 South Atlantic, 213–26 See also fisheries, commercial; country names longnose pygmy shark (Heteroscymnoides marleyi), 19 longnose skate (Raja rhina), 464 mackerel sharks. See Lamniformes (mackerel sharks) mako sharks. See longfin mako, shortfin mako Malaysia commercial fisheries of, 172, 177, 183, 186 management in, 426, 434, 436 NPOA development in, 482, 484 recreational fisheries in, 201 Maldives NPOA development in, 482, 484 fisheries of, 172, 177, 183–84, 186 recreational fisheries in, 201 shark bycatch of, 248 Malta: management in, 436 management, 418–39 bycatch data reporting and, 400 catch limits and, 395 catches and, 165, 167–68 comparative life history and, 309, 316–18 cooperative, 395, 418, 438 demographic analysis and, 352, 354 difficulties in, 6, 418–19, 437 domestic, 419, 421–22, 433–38, 434 ecosystem-based, 8 genetic population structure and, 323 in Hawaii, 268–73 Indian Ocean fisheries and, 254–55 international, 418–19, 425–28 International Plan of Action–Sharks and, 430, 478–489 lack of data and, 418–19, 437 National Shark Longline Management Plan (Papua New Guinea), 436 need for, 4–6 political will and, xxv, 485–87 recommendations for, 419, 438–39 regional, 419, 425 resources for, 486–87 RFMOs and, 5, 8, 420, 426–27, 428–30 shark finning and, 8, 395–96, 419, 420–23, 428, 429, 435 species protections and, 8, 423–25 status of, 437–38 stock assessment and, 351, 352–55 technology and, 396, 486 time and area closures and, 165 tools for, 419–25 wildlife conservation agreements and, 430–33 See also fisheries, commercial; country names; individual regional fisheries management organizations; shark names Marine Recreational Fisheries Statistics Survey (MRFSS), 198, 199, 205–11 Markov Chain Monte Carlo algorithm, 363 matrix population model, 310 Mauritania: NPOA development in, 482, 484 Mauritius: recreational fisheries in, 193, 201

498

Index

maximum sustainable yield (MSY) biomass and, 285 carrying capacity and, 310 mortality rates and, 285, 298 stock structure and, 286 rebound potential and, 298 Megachasmidae. See megamouth shark megamouth shark (Megachasma pelagios), 15, 16, 17, 21 Mexico, 275–81 artisanal fishery in, 276–77 commercial fisheries of, 166, 172, 177, 186, 275–81 management in, 426, 434, 435, 436 NPOA development in, 482 recreational fisheries in, 193, 201 regulations in, 279–80 shark finning and, 171, 422 shrimp trawl bycatch in, 278 stock assessment in, 278–79 migration genetic population structure and, 286, 324 reproduction and, 25, 57 segregation by sex and age and, 57 See also movements Mitsukurinidae. See goblin shark (Mitsukurina owstoni) molecular markers, 325–28 Monte Carlo simulations, 309, 310, 311, 356–57 mortality rates, xxiv, 301 bycatch, 462–70 demographic analysis and, 6, 285 maximum sustainable yield and, 285, 298 natural, 6, 74, 298 rebound potential and, 298, 305 recreational fisheries and, 201–2, 399 shark finning and, 8 tagging studies and, 387–88 movements, xxiv reproduction and, 213, 224–25 stock assessment and, 369 tagging studies and, 386–87 See also migration; shark names Mozambique, 177 MRFSS. See Marine Recreational Fisheries Statistics Survey Myanmar: NPOA development in, 482, 484 NAFO. See Northwest Atlantic Fisheries Organization Namibia commercial fisheries of, 173, 214, 216 management in, 436 NPOA development in, 482, 484 shark finning and, 8, 422 natal philopatry, 286 National Marine Fisheries Service (NMFS), 153, 205, 242, 425 Cooperative Shark Tagging Program of, 117, 131, 198, 199, 237, 339, 340 genetic identification and, 336 stock assessment and, 361 National Plan of Action for Sharks (NPOA–Sharks), 426–27, 434, 435, 478–92, 481 Netherlands, The, 177 Newfoundland, 339, 345, 447 New Zealand, 31, 33, 370, 409 commercial fisheries of, 172, 177, 184, 185, 186 domestic management action in, 433 management in, 427, 432, 434, 435, 436 NPOA development in, 482 recreational fisheries in, 193, 194, 197–98, 399 Nicaragua: shark finning and, 8, 422 Nigeria commercial fisheries of, 172, 178, 184, 186 management in, 427, 434 NPOA development in, 482 night shark (Carcharhinus signatus), 18 discards of, 163 commercial fisheries and, 222, 242, 244, 245

recreational fisheries and, 199 reproduction in, 24, 29, 32, 35, 38, 39, 40 North East Atlantic Fisheries Commission (NEAFC), 421 Northern Mariana Islands (NMI), 268 Northwest Atlantic Fisheries Organization (NAFO), 428 management and, 8 shark finning and, 8, 421 Norway, 339, 347 commercial fisheries of, 173, 178 NPOA–Sharks. See National Plan of Action for Sharks nurse shark (Ginglymostoma cirratum), 329 Ocean Wildlife Campaign, 4 Oceanic Fisheries Programme (OFP), 174, 175 oceanic sharks. See open ocean sharks oceanic whitetip shark (Carcharhinus longimanus), 5 abundance of, 128–29, 395 age and growth of, 132–33, 132 biology and ecology of, 15, 18, 128–37 catch rates (CPUE) and trends for, 130, 134–36, 136, 175, 251, 254, 403, 407–8 commercial fisheries and, 167, 167, 171, 174, 176, 177–78, 214, 215, 242, 243, 244, 245, 261, 269, 276, 465 conservation status of, 136–37, 174, 397, 401, 407–8, 411 diet of, 129, 131 distribution of, 57, 129–30, 130 ICCAT data collection on, 473 life-history parameters of, 311, 312, 314, 317 management of, 136–37, 272, 424, 432 movements of, 130–31 productivity of, 293, 398 rebound potential of, 291 recreational fisheries and, 198, 199 reproduction in, 24, 29, 32, 35, 38, 39, 40–41, 58, 129, 131–32 segregation by sex and age of, 57, 129 shark finning and, 135–36 species protections and, 424 wildlife conservation agreements and, 432 Odontaspididae (sand tiger sharks), 16, 17 OFP. See Oceanic Fisheries Programme Oman: shark finning and, 8, 422 open ocean sharks abundance of, xxiv, 164–65 age and growth of, 88 apex predators, 4, 5, 57, 330 biology and ecology of, xxiv–xxv, 4, 14–22, 57–59 catch and catch-rate data for, 163–65 coastal sharks vs., 14 conservation status of, xxv, 395–96, 397–411 demographic analysis of, 285, 298–306, 309–19 diet of, 4, 57 distribution of, xxv, 15–16, 323–30 extinction and, 7, 10 genetic population structure of, 323–30, 328–29 intrinsic rates of increase in, 288–94 knowledge gap and, 8, 10 life-history parameters of, xxiv, xxv, 7, 24, 57–58, 309–19 migration and, xxv, 3 movements of, xxiv, 57 productivity of, 285, 288–94, 298–306, 398 rebound potential of, 298–306 recreational fisheries and, 193–202 research and, 4–8 stock assessment of, 351–64 stock structure of, 286 See also management; shark names Orectolobiformes (carpet sharks), 14, 15, 16 Pacific cod (Gadus macrocephalus), 464 Pacific halibut (Hippoglossus stenolepis), 462, 464 Pacific Ocean, xxv blue shark in, 7 commercial fisheries in, 170, 171, 174–75, 175, 176–186, 260–67, 268–273, 275–81

Index

recreational fisheries in, 193–200 management in, 420–37, 482–83, 488 shark finning bans in, 8, 421–22 See also catch rates (CPUE) and trends Pacific sharpnose shark (Rhizoprionodon longurio), 276 Pakistan commercial fisheries of, 166, 172, 176, 178, 180, 186 management in, 426, 434 NPOA development in, 482 shark bycatch of, 248 Palau, 422, 425, 432 shark finning and, 8, 422 Panama: shark finning and, 422 Papua New Guinea: management in, 433, 434, 436 pelagic elasmobranches. See open ocean sharks pelagic stingray (Pteroplatytrygon violacea), 5, 20, 21 abundance of, 395 age and growth of, 152, 153–55, 154, 156 biology and ecology of, 15, 152–58, 153 bycatch, 152 catch rates (CPUE) and trends for, 404, 409 commercial fisheries and, 167, 167 conservation status of, 157, 401, 409 diet of, 152, 155 distribution of, 57, 155, 156 ICCAT data collection on, 288, 473 management and, 409, 424, 434 movements of, 157, 292 productivity of, 293, 294, 398 rebound potential of, 291, 292 reproduction in, 24, 26–27, 28, 29, 35, 41–43, 152, 155, 158 species protections and, 424 threats to, 157 pelagic thresher shark (Alopias pelagicus), 5 abundance of, 395 age and growth of, 62–64, 62 biology and ecology of, 15, 16, 17, 60–65 catch rates (CPUE) and trends for, 250, 251, 402, 403 commercial fisheries and, 65, 167, 176, 177–78, 261, 276 conservation status of, 397, 399, 401, 402, 411 demographic analysis of, 310 diet of, 21, 64–65 distribution of, 57, 60–61 fecundity of, 167, 309 genetic population structure of, 326 ICCAT data collection on, 473 life-history parameters of, 311, 312, 314, 317 management and, 65, 272, 424, 433, 434 movements of, 61 productivity of, 285, 293, 309, 398 rebound potential of, 193, 285, 291 recreational fisheries and, 194, 198, 200 reproduction in, 24, 28, 29, 30, 32, 34, 35, 58, 64 segregation by sex and age of, 63 shark finning and, 7 species protections and, 424 stock structure of, 62 wildlife conservation agreements and, 432 Peru commercial fisheries of, 172, 184, 186 NPOA development in, 482 shark finning and, 171 Philippines commercial fisheries of, 178 NPOA development in, 482, 484 recreational fisheries in, 201 pocket shark (Mollisquama parini), 19 population decline in, 7 demographic analysis and, 285, 298–306, 310, 354 density dependence and rebound potential of, 285 exploitation and, 309 genetic population structure, 323–30 inflection points and, 313–14

499

intrinsic rates of increase in, 44, 288–94 life-history parameters and, 309, 310, 316–19 of Northwest Atlantic porbeagle, 5 rebound potential of, 288–94, 298–306 survival rates and, 285 population dynamics analysis, 6 Bayesian methods, 359–64 catch-rate data and, 450, 451, 452 length and age composition trends and, 449–50 mortality rates and, 450–53 yield per recruit and, 454–55 stock assessment and, 351–59 stock structure and movement in, 369–89 population status. See conservation status porbeagle shark (Lamna nasus), 5, 411 abundance of, 106, 111, 445, 453–54 age and growth of, 105, 107, 109–10 biology and ecology of, 15, 17, 105–11 catch rates (CPUE) and trends for, 111, 168, 171, 172, 220, 260, 263, 403, 406–7, 445–46, 450, 451, 452 commercial fisheries and, 5, 167, 167, 171, 173, 173, 176, 177–78, 214, 218, 253, 260, 261, 261, 263, 446–55, 447, 449 conservation status of, 111, 397, 399, 401, 406–7, 411 diet of, 110 distribution of, 57, 106–7 exploitation rates for, 453–54 genetic population structure of, 328 ICCAT data collection on, 473, 474 length and age composition trends for, 449–50 life-history parameters of, 5, 108, 311, 312, 314, 317, 319 management and, 106, 110, 396, 406, 423, 424, 425, 430, 431–32, 433, 434, 435, 437, 459 migration of, 57 mortality rates for, 450–53 population dynamics analysis of, 445–59 productivity of, 105, 293, 398 rebound potential of, 291 recreational fisheries and, 110, 193, 196, 200, 448 reproduction in, 24, 29, 31–32, 32, 33, 35, 36, 105, 110, 406 salmon shark vs., 95–96 species protections and, 424 stock assessment of, 395, 400 stock structure of, 106–7, 111 tagging studies of, 106–7 wildlife conservation agreements and, 431–32, 432 yield per recruit and, 454–55 Portugal management in, 427, 434 commercial fisheries of, 168, 172, 178, 184–85, 186 NPOA development in, 482, 484 swordfish longline fishery catch-rate patterns in, 230–34 principal component analysis (PCA), 310–11 productivity demographic analysis and, 285, 298–306 intrinsic rates of increase and, 288–94 litter size and, 3 oceanic vs. coastal waters and, 3 reproduction in, 30 Pseudocarchariidae (crocodile sharks), 16, 17 pygmy shark (Euprotomicrus bispinatus), 19, 21 Rajiformes (batoids), 14, 15, 15, 20 rasptooth dogfish (Miroscyllium sheikoi), 19 rebound potential, 298–306, 300, 301, 304, 305 age and mortality and, 298 collapse threshold and, 302, 304, 305, 306 demographic analysis and, 298 fecundity and, 299, 301 maximum sustainable yield and, 301–2 mortality for MSY and, 302, 303, 305 parameters of, 299–301 population size for MSY and, 301–2

500

Index

rebound potential (Contd.) recovery time and, 304, 306 reproductive protection and, 302–3, 304, 306 recreational fisheries. See fisheries, recreational red drum (Sciaenops ocellatus), 325 Red List of Threatened Species (IUCN), xxiv, 76, 124, 137, 397, 400, 401, 402, 405–10, 432 regional fisheries management organizations (RFMOs), 5, 429 Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR), 428, 429 Commission for the Conservation of Southern Bluefin Tuna (CCSBT), 429 conservation and, 400 effectiveness of, 438 General Fisheries Commission of the Mediterranean (GFCM), 429 Indian Ocean Tuna Commission (IOTC), 8, 169, 176, 247, 248, 421, 426–27, 429, 488 Inter-American Tropical Tuna Commission (IATTC), 8, 124, 174, 175, 395, 421, 428, 429, 488 International Commission on the Conservation of Atlantic Tunas (ICCAT), 8, 91, 124, 136, 147, 169, 172, 174, 186, 214, 216, 395, 400, 421, 423, 426–27, 429, 472–77, 488 IPOA–Sharks and, 487–88 management and, 8, 426–27, 429 Northwest Atlantic Fisheries Organization (NAFO), 8, 421, 428 shark finning and, 6–7, 9, 420, 421, 423, 428, 429 Western and Central Pacific Fisheries Commission (WCPFC), 169, 174, 395, 421, 426–27, 428, 429 reproduction, 24–45 age and size at maturity, 24, 25, 34–36, 35, 39–40, 42, 44, 87 aplacental viviparity, 24, 58, 64 aplacental viviparity with oophagy, 26, 28, 87, 89 aplacental viviparity with trophonemata, 26–27, 42–43, 58 birth size and, 24, 25, 28, 30–31, 38–39, 41, 42–43 coastal sharks, 27 development and, 24 egg laying, 3 embryonic development, 25, 36–37, 42–43 embryonic oophagy, 24 environment and, 119 fecundity and, 27, 30, 58 gestation period, 24, 25, 27, 28, 31–32, 32, 39, 41–43, 64, 69 habitat and, 27, 28 Lamniformes, 28–37 litter size, 3, 24, 25, 27, 28–30, 37–38, 41, 42–43, 58, 64, 69, 74–75, 87 management and, 44 migration and, 25, 57 modes of, 25–27 movements and, 213, 224–25 oophagy, 37 oviparity, 25–27, 58 parturition and, 32, 33, 42–43, 75, 119 placental viviparity, 3, 24, 26, 28, 58, 119 reproductive periodicity, 24, 31, 32–34, 39, 42 resting period, 32 seasonality and, 25, 31, 33–34, 64 trends in, 27–28 viviparous, 24, 25–27 von Bertalanffy growth equation and, 30, 31, 34, 40 See also shark names reproductive protection collapse threshold and, 302, 304, 306 rebound potential and, 302–3 Republic of the Congo, 425 requiem sharks. See Carcharhinidae rig shark (Mustelus lenticulatus), 197 rockfish (Sebastes), 464

sablefish (Anoplopoma fimbria), 462, 464 salmon shark (Lamna ditropis), 5 abundance of, 395 age and growth of, 95, 96–97 biology and ecology of, 15, 17, 95–101, 96 body temperature of, 57, 95, 97 bycatch species, 95, 98–99, 100–101 catch rates (CPUE) and trends for, 269, 403, 407, 410 commercial fisheries and, 167, 167, 100–101, 179, 182, 269 conservation status of, 101, 395, 401, 407 diet of, 97 distribution of, 57, 95, 96, 98 genetic population structure of, 328 management and, 95, 101, 272, 424, 433 migration of, 57 mortality rates for, 95 movements of, 95, 98–100 porbeagle vs., 95–96 productivity of, 293, 398 rebound potential of, 291 recreational fisheries and, 193, 199 reproduction in, 24, 29, 30, 32, 32, 33, 35, 58, 96–97 segregation by sex and age of, 57, 95, 98–100, 98, 101 species protections and, 424 stock structure of, 95, 100 tagging studies of, 99–100, 99 sand tiger shark (Carcharias taurus) 16, 17, 37 productivity of, 293 rebound rates of, 291 sandbar shark (Carcharhinus plumbeus), 18 bycatch and, 243, 244, 245 465 intrinsic rates of increase for, 289, 362 productivity of, 293 rebound potential of, 292 species identification of tissues of, 334, 335, 336 stock assessment of, 361 scalloped hammerhead (Sphyrna lewini) fisheries and, 243, 244, 245, 465 productivity of, 293 rebound potential of, 292 Schnute models, 141 school shark (Galeorhinus galeus), 197, 357 Australian tuna longline fisheries and, 261 diet of, 370–73 distribution of, 369–70 mortality rates of, 380, 384 movements of, 369, 370, 373–74, 380, 381 productivity of, 293 rebound potential of, 291 reproduction in, 373 stock assessment of, 286, 373, 374–84 stock structure of, 369, 373–74 Scotland, 347 SEAFDEC. See Southeast Asian Fisheries Development Center SEAFO. See Southeast Atlantic Fisheries Organization Secretariat of the Pacific Community (SPC), 169, 174 semipelagic sharks, 14 Senegal: NPOA development in, 482, 484 sevengill shark (Notorynchus cepedianus), 291, 293 Seychelles commercial fisheries of, 178 finning prohibition and, 8, 422 NPOA development in, 481, 482 recreational fisheries in, 201 shark bycatch of, 250 shark fins: genetic identification and, 334–37 shark fin trade, 167, 170–72, 172, 395–96 Hong Kong and, 7, 166, 168, 173, 340, 399, 409–10, 431 shark finning, 8, 9, 110, 169, 184, 255, 270, 272, 273, 280, 395, 410, 411, 418–23, 421–22, 428, 429, 434, 435, 436, 437, 438, 476, 485, 488 Sherwood dogfish (Scymnodalatias sherwoodi), 19 shortbill spearfish (Tetrapturus angustirostris), 466 shortfin mako (Isurus oxyrinchus), 5

Index

abundance of, 153, 395 age and growth of, 88, 133 biology and ecology of, 15, 17, 87–91 catch rates (CPUE) and trends for, 7, 58, 91, 164–65, 205–8, 209, 210, 220, 222, 250, 251, 252, 260, 263, 268–71, 270, 403, 405–406, 473–77 commercial fisheries and, 87, 163, 167, 168, 171, 172, 173, 174, 176, 177–78, 214, 215, 218, 221, 242, 243, 244, 245, 260, 261, 261, 269, 276, 465 conservation status of, 87, 90–91, 395, 397, 399, 400, 401, 405–6, 411 diet of, 57, 89 distribution of, 87, 89 genetic population structure of, 286, 326, 328–29 ICCAT assessment of, 473, 474–76 life-history parameters of, 88, 311, 312, 314, 319 management and, 272, 422, 424, 429, 430, 432, 433, 434, 435, 436 migration of, 57 movements of, 89–90, 117 population assessments for, 91 productivity of, 293, 398 rebound potential of, 300 recreational fisheries and, 58, 87, 90–91, 193, 194, 196, 198, 199, 200, 205–11 reproduction and, 24 reproduction in, 24, 28, 29, 30, 31, 32, 33, 34, 35, 36, 58, 88, 89 shark finning and, 6, 7 species identification of tissues of, 334, 335 species protections and, 424 stock assessment of, 395, 400 stock structure of, 57, 91 tagging studies and, 57 threats to, 90–91 wildlife conservation agreements and, 432 Sierra Leone: NPOA development in, 482, 484 silky shark (Carcharhinus falciformis), 5, 21 abundance of, 395 age and growth of, 121–22, 121, 122, 133 biology and ecology of, 15, 17, 18, 114–25 biomass of, 18 catch rates (CPUE) and trends for, 7, 124, 175, 251, 253–54, 403, 407 commercial fisheries and, 4, 17, 163, 167, 171, 174, 176, 177–78, 214, 222, 242, 243, 244, 245, 247, 251, 253–54, 261, 269, 276, 465 conservation status of, 124–25, 174, 401, 407, 411 diet of, 122 distribution of, 57, 115, 116 genetic studies of, 119 ICCAT data collection on, 473 life-history parameters of, 120, 311, 312, 314, 317 management and, 124, 272, 424, 435, 436 migration of, 57 movements of, 117 productivity of, 293, 398 rebound potential of, 291 recreational fisheries and, 198 reproduction in, 24, 29, 32, 35, 38–39, 40–41, 58, 114–25, 119–21 segregation by sex and age of, 115 shark finning and, 7 species identification of tissues of, 334, 335 species protections and, 424 stock structure of, 117, 119, 123–24 tagging studies of, 118 threats to, 122–23 silvertip shark (Carcharhinus albimarginatus), 17, 252 Indian Ocean catch-rate data for, 253–54 Singapore commercial fisheries of, 178 shark finning and, 171 skipjack tuna (Katsuwonus pelamis), 469

501

rebound potential of, 300, 303 sleeper shark (Somniosus pacificus), 101 smalleye pygmy shark (Squaliolus aliae), 19 smalltooth sand tiger shark (Odontaspis ferox), 16, 17 smooth lanternshark (Etmopterus pusillus), 19 soaking times, 466 Solomon Islands: commercial fisheries of, 178 Somniosidae (sleeper sharks), 19 South Africa, 33, 339, 370 commercial fisheries of, 178, 214, 216 management in, 433, 434, 436 Natal Sharks Board, 247, 248 NPOA development in, 482 recreational fisheries in, 193, 194, 201, 436 shark bycatch of, 251 shark finning and, 8, 422 shark longline records from, 247 South China cookiecutter shark (Isistius labialis), 19 Southeast Asian Fisheries Development Center (SEAFDEC), 484 Southeast Atlantic Fisheries Organization (SEAFO), 8, 421 southern bluefin tuna (Thunnus maccoyii), 260–61, 300 Spain commercial fisheries of, 166, 168, 172, 173, 176, 178, 181, 186, 214, 216 finning prohibitions in, 422 management in, 426, 434, 436 NPOA development in, 482, 484 shark bycatch of, 248 shark finning and, 8, 171 sparsetooth dogfish (Scymnodalatias oligodon), 19 SPC. See Secretariat of the Pacific Community Species at Risk Act, 425 sphyrnid sharks, 292 spined pygmy shark (Squaliolus laticaudus), 19 spinner shark (Carcharhinus brevipinna), 17 spiny dogfish (Squalus acanthias), 18–19, 197, 198, 459, 464 intrinsic rates of increase for, 289 movements of, 373 productivity of, 293 rebound potential of, 300, 303–4, 306 rebound rates of, 291 Squaliformes (dogfish sharks), 14, 15, 15, 18–19 squid, 4, 57 Sri Lanka commercial fisheries of, 166, 172, 178, 181, 186 management in, 426, 434, 436 NPOA development in, 482 shark bycatch of, 248, 250 starfish (Astropectin spp.), 469 stock assessment, 353 Bayesian methods and, 351, 359–64 bycatch data reporting and, 400 catch-rate data and, 355–56 conservation and, 351 demographic analysis and, 352, 354 goals of, 351, 352 management and, 351, 352–55 Markov Chain Monte Carlo algorithm and, 363 movements and, 369 population dynamics model and, 6, 358 requirements for, 351, 352 spatially structured, 374–84 surplus production models and, 354–55 tagging studies and, 374–84 teleost fish and, 351 uncertainty and problems with, 355–59 stock structure bigeye thresher, 62 common thresher, 62 genetic, 323–30 impact of fishing and, 286 mathematical models for assessing, xxv, 286 maximum sustainable yield and, 286

502

Index

stock structure (Contd.) open ocean sharks, 286 pelagic thresher, 62 tagging studies and, 325 striped marlin (Tetrapturus audax): rebound potential of, 300 swordfish (Xiphias gladius), 163, 216, 230–34, 300, 462, 465 tagging studies growth and, 387–88 knowledge gap and, 10 likelihood function and, 386 mortality rates and, 387–88 movement and survival and, 386–87 North Atlantic blue shark stock structure and, 339–48 pop-up satellite, 82–83, 100 recreational fisheries and, 193, 197 stock assessment and, 374–84 stock structure and, 325 tag survival ratio and, 385–86 taillight shark (Euprotomicroides zantedeschia), 19, 21 Taiwan commercial fisheries of, 166, 172, 176, 178, 181–82, 186, 214, 215–16 management in, 426, 434, 436 NPOA development in, 482 shark bycatch of, 249 shark finning and, 171, 434 Tanzania: commercial fisheries of, 178 teleost fish, 57 intrinsic rates of increase for, 288 productivity of, 294 rebound potential of, 300, 303–4 stock assessment and, 351 Thailand commercial fisheries of, 172, 178, 185, 186 management in, 426, 434 NPOA development in, 482, 484 recreational fisheries in, 201 shark bycatch of, 248 thorny stingray (Dasyatis centroura), 158 thresher sharks. See bigeye thresher; common thresher; pelagic thresher tiger shark (Galeocerdo cuvier), 6, 18 commercial fisheries and, 243, 244, 245, 261, 269, 276, 465 movements of, 117 productivity of, 293 rebound rates of, 292 reproduction in, 37 tournaments, 197, 205–9 TRAFFIC International, 183, 478 Turkey: commercial fisheries of, 178 UN Conference on Straddling Fish Stocks and Highly Migratory Fish Stocks (1995), 480 UN Convention on the Law of the Sea (UNCLOS), 425, 428, 437, 438 UN Driftnet Ban, 425 UN Fish and Stocks Agreement (UNFSA), 425, 428, 438 UN General Assembly (UNGA), 419, 421, 485 United Arab Emirates (UAE): shark finning and, 171 United Kingdom, 370 commercial fisheries of, 172, 178, 186 management in, 427, 434 NPOA development in, 483, 484 recreational fisheries in, 193, 194, 200, 399 United States commercial fisheries of, 165, 166, 172, 173, 178, 182, 185, 186, 242–45, 268–73 management in, 422, 426, 433, 434, 437 NPOA development in, 481, 483 recreational fisheries in, 193, 194, 198–200, 205–11, 399, 433 shark finning and, 8, 171, 422, 423

Uruguay, 163, 370 catch-rate trends and, 165, 214, 216–19, 217, 218, 220 commercial fisheries of, 178 NPOA development in, 483 velvet dogfish (Zameus squamulosus), 19, 215, 473 fisheries and, 214, 221, 261 Venezuela: NPOA development in, 483 Vietnam: NPOA development in, 483, 484 viper dogfish (Trigonognathus kabeyai), 19 von Bertalanffy growth equation, 30, 31, 34, 40, 60, 69, 73, 109, 121, 132, 311 wahoo (Acanthocybium solandri), 465 Western and Central Pacific Fisheries Commission (WCPFC), 395 bycatch and, 169, 174, 185 management and, 421, 426–27, 428, 429 shark finning and, 421, 429 whale shark (Rhincodon typus), 16, 21 management of, 423 wildlife conservation agreements and, 432 white marlin (Tetrapturus albidus), 466 white shark (Carcharodon carcharias), 5 abundance of, 76, 395 age and growth of, 69, 72–74, 73 apex predators, 82 Barcelona Convention and, 437 biology and ecology of, 15, 17, 69–76 birth size of, 73 catch rates (CPUE) and trends for, 76, 252, 403, 405 CITES and, 437 CMS (Bonn Convention) and, 437 commercial fisheries and, 167, 167, 168, 171, 177–78 conservation status of, 70, 75–76, 397, 401, 405, 411 diet of, 57, 75 distribution of, 70 effects of temperature on, 71–72 genetic analysis of, 70, 328 management and, 395, 424, 425, 431–32, 433, 434, 435, 436–37 migration of, 3, 5, 57 mortality rates and, 74 movements of, 71, 82–84, 83 productivity of, 293, 398 protected status of, 395 rebound potential of, 291, 300 recreational fisheries and, 194, 196 Red List of Threatened Species and, 76 reproduction in, 24, 29, 30, 31, 32, 32, 33–34, 35, 36, 37, 58, 69, 74–75 segregation by sex and age of, 70 species protections and, 424, 425 stock structure of, 69, 72, 328 tagging studies of, 70, 71, 82–83, 83 wildlife conservation agreements and, 432 whitetail dogfish (Scymnodalatias albicauda), 19, 21 whitetip reef shark (Triaenodon obesus), 292, 293 wildlife conservation agreements, 430–33 CMS (Bonn Convention), 432–33 Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), xxiv, 76, 168, 169, 186, 398, 430, 431–32, 439, 472, 479–80, 481–83, 488 World Conservation Union (IUCN), 186 IPOA–Sharks and, 478 Red List of Threatened Species of, xxiv, 76, 124, 137, 397, 400, 401, 402, 405–10, 432 shark finning and, 421 Shark Specialist Group (SSG) of, 400, 402, 478, 481 yellowfin tuna (Thunnus albacores), 465 rebound potential of, 300, 303 Yemen: management in, 427, 434